Oxford Series in Ecology and Evolution

Edited by Paul H. Harvey, Robert M. May, Charles H. Godfray, and Jennifer A. Dunne

The Comparative Method in Evolutionary Biology

Paul H. Harvey and Mark D. Pagel
The Cause of Molecular Evolution
John H. Gillespie
Dunnock Behaviour and Social Evolution
N. B. Davies
Natural Selection: Domains, Levels, and Challenges
George C. Williams
Behaviour and Social Evolution of Wasps: The Communal Aggregation Hypothesis
Yosiaki Itô
Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology
Eric L. Charnov
Quantitative Ecology and the Brown Trout
J. M. Elliott
Sexual Selection and the Barn Swallow
Anders Pape Møller
Ecology and Evolution in Anoxic Worlds
Tom Fenchel and Bland J. Finlay
Anolis Lizards of the Caribbean: Ecology, Evolution and Plate Tectonics
Jonathan Roughgarden
From Individual Behaviour to Population Ecology
William J. Sutherland
Evolution of Social Insect Colonies: Sex Allocation and Kin Selection
Ross H. Crozier and Pekka Pamilo
Biological Invasions: Theory and Practice
Nanako Shigesada and Kohkichi Kawasaki
Cooperation Among Animals: An Evolutionary Perspective
Lee Alan Dugatkin
Natural Hybridization and Evolution
Michael L. Arnold
Evolution of Sibling Rivalry
Douglas Mock and Geoffrey Parker
Asymmetry, Developmental Stability, and Evolution
Anders Pape Møller and John P. Swaddle
Metapopulation Ecology
Ilkka Hanski
Dynamic State Variable Models in Ecology: Methods and Applications
Colin W. Clark and Marc Mangel
The Origin, Expansion, and Demise of Plant Species
Donald A. Levin
The Spatial and Temporal Dynamics of Host-Parasitoid Interactions
Michael P. Hassell
The Ecology of Adaptive Radiation
Dolph Schluter
Parasites and the Behavior of Animals
Janice Moore
Evolutionary Ecology of Birds
Peter Bennett and Ian Owens
The Role of Chromosomal Change in Plant Evolution
Donald A. Levin
Living in Groups
Jens Krause and Graeme Ruxton
Stochastic Population Dynamics in Ecology and Conservation
Russell Lande, Steiner Engen and Bernt-Erik Sœther
The Structure and Dynamics of Geographic Ranges
Kevin J. Gaston
Animal Signals
John Maynard Smith and David Harper
Evolutionary Ecology: The Trinidadian Guppy
Anne E. Magurran
Infectious Diseases and Primates Socioecology
Charles L. Nunn and Sonia M. Altizer
Computational Molecular Evolution
Ziheng Yang
The Evolution and Emergence of RNA Viruses
Edward C. Holmes
Aboveground–Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global
Change
Richard D. Bardgett and David A. Wardle
Aboveground–
Belowground Linkages
Biotic Interactions, Ecosystem Processes,
and Global Change

RICHARD D. BARDGETT
Soil and Ecosystem Ecology Laboratory, Lancaster
Environment Centre, Lancaster University, Lancaster, UK

DAVID A. WARDLE
Department of Forest Ecology and Management, Swedish
University of Agricultural Sciences, Umeå, Sweden

1
3
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1 3 5 7 9 10 8 6 4 2
Contents

Preface ix
1 Introduction 1
1.1 Controls on terrestrial ecosystem processes: an historical perspective 3
1.2 Species and biotic interactions as ecosystem drivers 5
1.3 Aboveground–belowground interactions as drivers of ecosystem
processes 8
1.4 Aboveground–belowground interactions and global change 10
1.5 Emerging issues and trends 12

2 Biotic interactions in soil as drivers of ecosystem

properties 15
2.1 Introduction 15
2.2 Influence of decomposers on aboveground communities and ecosystem
processes 17
2.2.1 Free-living soil microbes, nutrient availability, and plant growth 17
2.2.2 Trophic interactions in soil, nutrient availability, and plant growth 23
2.2.3 Functional consequences of trophic cascades in the soil food web 26
2.2.4 Bacterial-based and fungal-based energy channels and nutrient
cycling 28
2.3 Influence of root-associated organisms on plant communities and
ecosystem processes 32
2.3.1 Microbial symbionts and plant community dynamics 32
2.3.2 Belowground pathogens, herbivores, and plant community
dynamics 38
2.4 Soil ecosystem engineers and plant community dynamics 40
2.5 Soil biotic interactions, carbon dynamics, and global change 45
2.5.1 Soil biotic interactions and ecosystem carbon exchange 46
2.5.2 Contribution of soil biotic interactions to climate change via
carbon-cycle feedbacks 52
2.5.3 Multiple global change drivers and soil biotic interactions 57
2.6 Conclusions 59
vi • Contents

3 Plant community influences on the soil community and

plant–soil feedbacks 62
3.1 Introduction 62
3.2 How plants affect the belowground subsystem 63
3.2.1 Differential effects of different plant species 63
3.2.2 Effects of within-species variation 68
3.2.3 Spatial and temporal variability 70
3.2.4 Multiple species effects 72
3.3 Overriding effects of plant traits 75
3.3.1 Contrasting plant species and trait axes 75
3.3.2 Trait dominance, trait dissimilarity, and multiple species effects 81
3.3.3 Ecosystem stoichiometery 84
3.4 Plant–soil feedbacks 85
3.5 Succession and disturbance 90
3.5.1 The build-up phase of succession 91
3.5.2 Ecosystem retrogression 93
3.5.3 Succession and plant–soil feedbacks 97
3.6 Indirect belowground effects of global change via vegetation 99
3.6.1 Indirect belowground effects of climate change 99
3.6.2 Indirect belowground effects of nitrogen deposition 107
3.7 Conclusions 110

4 Ecosystem-level significance of aboveground consumers 113

4.1 Introduction 113
4.2 Herbivore-mediated effects on plant–soil feedbacks and ecosystem
processes 114
4.2.1 Positive effects of herbivores on belowground properties and
ecosystem functioning 116
4.2.2 Negative effects of herbivores on belowground properties and
ecosystem functioning 123
4.2.3 Landscape-scale herbivore effects and multiple stable states 130
4.3 The role of plant traits in regulating herbivore impacts 134
4.4 Aboveground trophic cascades and consequences for belowground
properties 137
4.5 Spatial movement of resources by consumer organisms 141
4.5.1 Resource transfers across land 142
4.5.2 Resource transfers from aquatic to terrestrial ecosystems 147
4.6 Aboveground consumers, carbon dynamics, and global change 152
4.7 Conclusions 161
 Contents • vii

5 Aboveground and belowground consequences of species

losses and gains 165
5.1 Introduction 165
5.2 Species losses through extinction and aboveground–belowground
linkages 166
5.2.1 The diversity-function issue from an aboveground–belowground
perspective 166
5.2.2 Removal experiments for studying effects of species losses 172
5.2.3 Effects of species losses in real ecosystems 180
5.3 Species gains through invasion and aboveground–belowground linkages 183
5.3.1 Invasions by plants 183
5.3.2 Belowground invaders 190
5.3.3 Invasions by aboveground consumers 195
5.4 Consequences of global change through causing species gains and losses 201
5.5 Conclusions 208

6 Underlying themes and ways forward 211

6.1 Introduction 211
6.2 Biotic interactions, feedbacks, and ecosystem processes 212
6.2.1 Linkages and feedbacks between the aboveground and
belowground subsystems 212
6.2.2 Organism traits as ecological drivers 214
6.3 Drivers of spatial and temporal variability 217
6.3.1 Drivers of variation over time 217
6.3.2 Drivers of variation over space 219
6.3.3 Differences across ecosystems 221
6.3.4 Global-scale contrasts 222
6.4 Global change phenomena 224
References 227
Index 289
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Preface

The principal aim of this book is to synthesize recent advances in our understanding
of interactions between aboveground and belowground communities, and how these
interactions regulate the functioning of terrestrial ecosystems and their responses to
global change. The last two decades, and especially the last 5 years, have witnessed
vastly increased activity on this topic, and as this has led to several important
conceptual advances in this field; hence, we felt that a comprehensive synthesis of
the topic would be timely. Even since we first began to plan this book, during a field
excursion in the mountains of New Zealand’s South Island in 2007, we have been
astonished by the growing number of studies emerging on this topic, several of which
have led to major leaps in conceptual understanding. As a consequence, during the
writing of this book we have had to constantly update chapters as new and important
studies have emerged. We have attempted to capture this recent and ongoing interest,
right up to the last day of writing in December 2009. If the recent and rapid
development of the topic does not leap out of these pages, then we have failed to
do it justice.
A key message of this book is that an improved understanding of how terrestrial
ecosystems function and respond to global change can be gained only by considering
the aboveground and belowground subsystems in tandem. We illustrate this by
considering four key aspects of aboveground–belowground linkages: biotic inter-
actions in the soil; plant community effects; the role of aboveground consumers; and
the influence of species gains and losses. We then draw together this information and
identify a number of cross-cutting themes, which include how aboveground–below-
ground feedbacks manifest themselves at vastly different spatial and temporal scales,
the consequences of these feedbacks for community and ecosystem processes, and
how aboveground–belowground interactions link to human-induced global change.
In doing so, we have attempted to identify areas of significant recent development as
well as productive avenues for future research. In writing this book, we have drawn
on literature from a wide range of disciplines and from studies that cross many types
of ecosystems around the world. However, it is not our intention to provide an
exhaustive analysis of the vast literature on aboveground–belowground linkages.
Rather, we have selected representative studies and examples to illustrate key con-
cepts and significant advances in this field, and to suggest interesting detours that the
reader may wish to explore themselves.
x • Preface

There are many people we would like to thank who helped us in various ways in
writing this book. First, we thank Robert May of Oxford University for originally
suggesting that we write the book, and Ian Sherman from Oxford University Press for
giving us the initial encouragement needed to get it off the ground. We are also most
grateful to Helen Eaton from Oxford University Press for her considerable assistance
throughout this endeavour, and for ensuring that the developmental process of this
book was smooth and problem-free. We are also very grateful to our many colleagues
who willingly provided us with in-depth comments on individual chapters and
portions of text, directed us towards additional relevant literature that we had missed,
and made constructive suggestions on improving the content as well as the clarity of
text. Colleagues who provided valuable feedback on various chapters include Hans
Cornelissen, Franciska de Vries, Doug Frank, Micael Jonsson, Paul Kardol, Marie-
Charlotte Nilsson, Kate Orwin, Heikki Setälä, Carley Stevens, Wim Van der Putten,
and Rene Van der Wal. We are also very grateful to the many colleagues with whom
we have each interacted over the past 20 or more years, too numerous to list here, who
have all contributed in multiple ways to the development of our own ideas, research
programs, and understanding of how terrestrial communities and ecosystems func-
tion. Without a range of interesting colleagues with whom to interact, collaborate, and
discuss, a book of this type could not have been written. Finally, we are indebted to
our families, and especially Jill and Anna, who supported, tolerated, and encouraged
us throughout the development and writing of this book.
Richard D. Bardgett
December 2009 and David A. Wardle
1
Introduction

Our understanding of how organisms, and their interactions with each other and their
abiotic environment, govern the functioning of terrestrial ecosystems has advanced
rapidly over the last two decades. This has been driven by a number of issues, the
most significant being the need to better understand the consequences for ecosystems
and the Earth-system of the dramatic changes in biological communities that have
resulted from human activity (Pimm et al. 1995; Vitousek et al. 1997c; Sala et al.
2000; Millennium Ecosystem Assessment 2005). An important development in this
area has been a growing recognition that terrestrial ecosystems consist of both
aboveground and belowground subsystems, and that feedbacks between these sub-
systems play a crucial role in regulating community structure and ecosystem func-
tioning (e.g. Hooper et al. 2000; Van der Putten et al. 2001; Wardle 2002; Wardle
et al. 2004a; Bardgett 2005). As a consequence, it is now widely understood that
biotic interactions between aboveground and belowground communities play a
fundamental role in regulating the response of terrestrial ecosystems and the Earth-
system to human-induced global change (Wolters et al. 2000; Wardle et al. 2004a;
Bardgett et al. 2008; Van der Putten et al. 2009).
The principal aim of this book is to synthesize recent advances in understanding of
the roles that biotic interactions between aboveground and belowground communi-
ties play in regulating the structure and function of terrestrial ecosystems, and the
response of ecosystems to global change. We also evaluate what can be learned from
the recent proliferation of studies on the ecological and biogeochemical significance
of biotic interactions between aboveground and belowground communities. In doing
so, we draw together a large body of literature that tackles this topic from a range of
perspectives and at vastly different spatial and temporal scales. These studies range
from those that explore the significance of root–microbial interactions for nutrient
acquisition and plant growth at the individual plant level, to those which examine
how biome-level shifts in vegetation composition resulting from global change
influence carbon-cycle feedbacks at a global scale. We do not aim to present new
facts, but we do attempt to bring some order and synthesis to the topic of above-
ground–belowground interactions as terrestrial ecosystem drivers.
There is no shortage of recent reviews on the topic of aboveground–belowground
interactions, including our own books (Wardle 2002; Bardgett 2005). However, these
books do not capture the many new insights into this topic that have emerged in the past
half-decade, and other recent overviews about aboveground–belowground interactions
2 • 1 Introduction

have generally focused on specific components of the topic, for example in the context
of multitrophic interactions (Scheu 2001; Van der Putten et al. 2001), herbivory
(Bardgett et al. 1998b; Bardgett and Wardle 2003), soil biodiversity (Hooper et al.
2000; De Deyn and Van der Putten 2005; Wardle 2006; Fierer et al. 2009), plant
community dynamics (Van der Putten 2003, 2009; Van der Heijden et al. 2008; Van
der Heijden and Horton 2009), ecosystem nutrient cycling and carbon dynamics
(Schimel and Bennett 2004; Bardgett et al. 2005; De Deyn et al. 2008; Frank and
Groffman 2009), and climate-feedback processes (Wardle et al. 1998c; Wolters et al.
2000; Bardgett et al. 2008; Wookey et al. 2009). Here, we bring such information
together to provide a comprehensive synthesis about the role of aboveground–
belowground interactions as terrestrial ecosystem drivers in a changing world.
The complexity of biotic interactions between aboveground and belowground
organisms, the interactions of these organisms with their abiotic environment, and
their variations in spatial and temporal scales at which they operate, is enormous
(Wardle 2002). Hence, we have divided the book into what we believe to be a logical
and palatable format. In the next three chapters we examine what we consider to be
the three main groups of biotic drivers of terrestrial ecosystem functioning: Chapter 2
focuses on the belowground consumers; Chapter 3 focuses on the plant community;
and Chapter 4 focuses on the aboveground consumers. Chapter 5 then draws upon the
concepts developed in these preceding chapters to examine how biotic interchange,
or human-induced species loss and gain, affects ecosystems through affecting
aboveground–belowground linkages. Finally, in Chapter 6 we bring together the
main threads from the preceding chapters to generate overall conclusions, emphasize
emerging developments, and highlight what we believe to be productive avenues for
future work. One important feature of the book is that the issue of global change is
considered in depth throughout all the chapters. This issue might have been con-
sidered as an individual chapter (as was done in Wardle 2002 and Bardgett 2005), but
given that global change is of fundamental importance to each of the three groups of
biotic drivers considered in this book, and that there has been a substantial body of
recent literature produced in this area, we argue that it is most effective to consider
each group separately in the context of global change.
The aim of this introductory chapter is to place our examination of aboveground–
belowground linkages in the broader context of ecosystem ecology, and explore the
historical development of this topic and its relationship to other fields of ecology. We
begin by providing a historical perspective on ecosystem ecology, emphasizing the
development of understanding of the role of abiotic and biotic drivers of ecosystem
processes. We then explore this theme further by considering developments in our
understanding of how species and species interactions act as important drivers of
ecosystem processes. Following this, we discuss more recent advances in the topic of
how interactions and feedbacks between aboveground and belowground biota may
serve as drivers of ecosystem processes. Finally, we place this discussion in a global
change context, by emphasizing how aboveground and belowground interactions
play a fundamental role in regulating the response of terrestrial ecosystems and the
Earth-system to human-induced global change.
 1.1 An historical perspective • 3

1.1 Controls on terrestrial ecosystem processes:

an historical perspective
Ecosystem science, which addresses the interactions between organisms and their
physical environment as an integrated system, is a relatively young discipline.
Indeed, the term ecosystem was not used in the literature until 1935, when the British
plant ecologist Arthur Tansley coined it to emphasize the importance of transfers of
materials between organisms and their abiotic environment (Tansley 1935). This
systems approach to studying ecosystems was further developed by Raymond
Lindeman, whose classic work on trophic dynamics and ecosystem energy flow
(Lindeman 1942) paved the way for many basic concepts in ecosystem ecology,
and by Eugene and Howard Odum who pioneered the use radioactive tracers to
document patterns of energy flow through ecosystems. Following this, Eugene Odum
published his classic strategy-based theory for understanding ecosystem development
(Odum 1969). Since this time, and especially during the last twenty years, the study
of ecosystem science has grown rapidly. Moreover, the growth of ecosystem-level
experiments, including whole-ecosystem manipulations (e.g. Likens et al. 1977;
Carpenter et al. 1985) and the use of well-defined environmental gradients (e.g.
Vitousek 2004), has served to greatly increase understanding of the factors that
regulate the structure and function of terrestrial ecosystems, and provide the basis
for critical decision-making based on ecosystem management. The demands of
global change and Earth-system research, which concerns human influences on
interactions among terrestrial ecosystems, the atmosphere, and the oceans, are likely
to increase the importance of ecosystem science in the future.
Another key step in ecosystem ecology was the development of the state factor
concept of Jenny (1941), which recognizes that the structure and function of terres-
trial ecosystems is governed by a set of state factors, namely climate, parent material,
topography, time, and biota. This concept has provided a logical framework for
ecologists to study the relative influence of each state factor on ecosystem processes,
thereby greatly advancing the field. For example, the chronosequence approach and
associated space-for-time substitution has been successfully used as a tool for
studying temporal dynamics of plant and microbial communities, soil development,
and ecosystem processes, as will be considered in Chapter 3 (e.g. Crocker and Major
1955; Whittaker 1956; Chapin et al. 1994; Crews et al. 1995; Wardle et al. 2004b;
Bardgett et al. 2007a). Likewise, different types of environmental gradients, for
example of topographic position, climate, and geologic substrate, have been used
to determine the relative role of landscape versus biotic controls, such as herbivory,
on ecosystem processes, as will be covered in Chapter 4 (e.g. Tracy and Frank 1998;
Augustine and McNaughton 2006; Anser et al. 2009). Meanwhile, climatic gradients
have been used to inform on the consequences for plant production and carbon
dynamics of woody plant invasion in grass-dominated ecosystems (e.g. Jackson
et al. 2002; Knapp et al. 2008), an issue that will be considered in Chapter 5. Another
related development is the recognition that natural ecosystems contain complex
networks of interacting feedbacks, which can strongly regulate the internal dynamics
4 • 1 Introduction

of terrestrial ecosystems (DeAngelis and Post 1991). For instance, and as will be
discussed in Chapter 3, there is now growing evidence that negative feedbacks, which
occur when two components of an ecosystem have opposite effects on one another,
play an important role in regulating the dynamics of plant communities (e.g. Bever
1994; Van der Putten et al. 1993; Klironomos 2002; Bezemer et al. 2006; Kardol et al.
2007). Likewise, positive feedbacks, such as those which operate between herbi-
vores, soil nutrient cycles, and plants, are now recognized as being key drivers of
ecosystem dynamics (McNaughton 1983, 1985; Bardgett et al. 1998b; Bardgett and
Wardle 2003). Further, carbon-cycle feedbacks between the land surface and atmos-
phere are increasingly seen as having major implications for the climate and Earth-
system (Jenkinson et al. 1991; Cox et al. 2000; Heimann and Reichstein 2008;
Chapin et al. 2009).
Although organisms and their interactions are fundamental to the concept of
ecosystem ecology, the inclusion of biotic interactions in ecosystem and Earth-
system science has been relatively recent. This most likely stems from community
and ecosystem ecology having to some extent developed independently of one
another. Here, community ecology has been primarily concerned with understanding
how communities are affected by environmental (e.g. climate, disturbance, and soil
fertility) and biotic factors (e.g. competition, predation, and mutualisms), while
ecosystem ecology has been mostly focused on studying rates and flows of energy
and nutrients within ecosystems. However, the last two decades have witnessed a
growing recognition of the roles that species play in ecosystems, and studies that
consider elements of both community ecology and ecosystem ecology are now
commonplace in the ecological literature. As will be discussed in the following
sections, this shift has been motivated by many factors, including a growing recog-
nition of the roles that aboveground and belowground biota and multitrophic inter-
actions play in driving ecosystem processes (Grime 1979; Coley et al. 1985; Lawton
and Jones 1995; van der Putten et al. 2001), and a vast research effort aimed at
connecting biodiversity to ecosystem functioning (Hooper et al. 2005). Further, the
growing desire to predict how species responses to global change influence ecosys-
tem processes such as decomposition and the cycling of nutrients has generated much
interest in the concept of functional classification, and especially the role of plant
species traits in ecosystem functioning (e.g. Grime 1998; Lavorel and Garnier 2002;
Vile et al. 2006; Diaz et al. 2007).
Another important development in ecosystem ecology has been in the use of
mathematical models to predict the consequences of changes in abiotic and biotic
conditions for ecosystem processes, including nutrient and carbon fluxes. For in-
stance, a number of modelling approaches have been developed for understanding the
controls on carbon cycling, ranging from global circulation models (GCMs) to soil-
carbon process models that can be parameterized at the plot, core, or microsite scale.
Further, progress has been made in coupling GCMs with dynamic global vegetation
models (DGVMs) for studying impacts of broad-scale shifts in vegetation (at the
level of coarse functional types) on feedbacks to the climate system. This has in turn
enabled simulation of impacts of climate change on vegetation cover and soil-carbon
 1.2 Species and biotic interactions • 5

storage (Cox et al. 2000; Sitch et al. 2003; Woodward and Lomas 2004). Also, while
most soil-carbon models have historically represented soil carbon as pools of organic
matter (Paustian 1994), attempts have been made to include more detailed under-
standing of the role of soil food webs in regulating soil-carbon fluxes. For example,
the pioneering soil food-web model developed by Hunt et al. (1987) for shortgrass
steppe in North America used functional groupings of soil organisms to calculate
carbon and nitrogen fluxes and rates of nitrogen mineralization. This model explicitly
incorporated estimates of various parameters for these organisms including their
carbon-to-nitrogen ratio, rate of turnover, assimilation and production efficiency,
and population size. This modelling has also been used to examine functional
responses of shifts in food-web energy channels (Moore and Hunt 1988) and the
ecosystem effects of losses of functional groups and their combinations within soil
food webs (Hunt and Wall 2002), as will be discussed in Chapter 2. There is still
much to be done to accurately represent biological interactions in ecosystem models
(Van der Putten et al. 2009), although such integration is crucial to improve predic-
tions of global change on ecosystem processes and feedbacks to the Earth-system.

1.2 Species and biotic interactions as ecosystem drivers

The issue of how species and differences among species affect ecosystems has been
long recognized by ecologists. For example, Müller (1884) proposed that plant
species and variants within plant species were powerful determinants of the types
of soils that develop under them (i.e. ‘mull’, ‘moder’ or ‘mor’), the soil invertebrate
communities that they support, and nutrient supply from the soil for plant growth.
Further, Handley (1954, 1961) performed a comprehensive series of experiments to
show that the ericaceous shrub Calluna vulgaris could form tannin–protein com-
plexes that reduce the availability of nitrogen to coexisting plant species. However,
despite this historical literature on how plant species differences affect ecosystems,
widespread recognition by ecologists that species effects are powerful ecosystem
drivers, or the question of ‘what do species do in ecosystems’ (Lawton 1994), is
comparatively recent. This topic has become an increasingly dominant theme in
ecology, especially following publication of the influential book Linking Species
and Ecosystems edited by Jones and Lawton (1995).
It has long been recognized that some species in a community have greater
effects on community or ecosystem properties than do others, either because they
simply produce more mass (i.e. dominant species) or because they have some
attribute that causes them to have disproportionate effects relative to their mass
(i.e. keystone species) (Paine 1969; Power et al. 1996). With regard to plant
communities, Grime (1998) proposed through his Mass Ratio Hypothesis that the
effects of each species in a community on ecological processes should scale with its
relative contribution to total community biomass. Conversely, there is strong
evidence that some plant species, notably those capable of symbiotic nitrogen
fixation, may substantially alter community and ecosystem properties even when
6 • 1 Introduction

occupying only a small proportion of total community biomass, as shown through

the classic work of Vitousek et al. (1987) and Vitousek and Walker (1989) on the
invasion of nitrogen-poor native forests of Hawai’i with the exotic nitrogen-fixer
Myrica faya. Differences between species on ecosystem properties are also appar-
ent through the rapidly expanding literature on plant strategies and traits. It has long
been recognized, including through the classic r-K continuum model (Macarthur
and Wilson 1967), that a fundamental trade-off exists between those organisms
with rapid growth rates which are adapted for resource acquisition, and those which
grow more slowly and are adapted for resource conservation. More complex models
for characterizing plant strategies and traits have since been developed, the best
known being the C-S-R (competitor, stress tolerator, ruderal) model of Grime
(1977). Subsequently, analysis of plant trait databases for large numbers of species
over regional or global scales (e.g. Grime et al. 1997; Díaz et al. 2004; Wright et al.
2004) has confirmed the existence of a primary axis of evolutionary specialization
that discriminates between species having traits suited for resource acquisition and
those suited for resource conservation. These traits are also increasingly recognized
as being important in determining differences between species in the quality
of resources that they produce, and ultimately their effects on ecosystem pro-
cesses, both aboveground and belowground (Wardle et al. 2004a), as we explore
in Chapter 3.
A major component of understanding how plant species differ in terms of their
ecosystem effects involves interspecific differences in plant litter quality: different
plant species differ greatly in terms of the decomposability of their litter by soil
microbes and fauna, and the pattern of nutrient release from this litter. This in turn
has a major influence on nutrient cycling and plant nutrition, soil organic-matter
formation and dynamics, the quality of soil organic matter, communities of soil
organisms, and ecosystem carbon storage. There is a long history of work on this
topic, which has gained increasing attention from soil biologists and ecosystem
scientists, especially following publication of the influential synthesis Decompos-
ition in Terrestrial Ecosystems by Swift et al. (1979). As such, there has been much
interest in the chemical and physical controls of decomposition and nutrient min-
eralization of plant litter (e.g. ratios of carbon to nutrients or nutrients to lignin;
concentrations of lignin or polyphenolics), and how this varies among species (e.g.
Taylor et al. 1989; Berg and Ekbohm 1991). The issue of plant-litter quality as an
ecological driver gained renewed vigour at around the time of publication of the
book Driven by Nature: Plant Litter Quality and Decomposition edited by Cadisch
and Giller (1997). As such, the past 15 years have witnessed a sharp increase in
recognition of the importance of plant traits (notably those that distinguish species
with a resource-acquisitive strategy in contrast to those with a conservative strat-
egy) as powerful drivers of litter quality and ecosystem processes driven by litter
quality (e.g. Cornelissen 1996; Grime et al. 1996; Wardle et al. 1998a; Cornwell
et al. 2008; Fortunel et al. 2009).
Another aspect of how plant species and traits affect ecosystem properties is
through their interactions with herbivores. There is a long history of trophic
 1.2 Species and biotic interactions • 7

dynamic theory regarding how herbivores and their predators both respond to and
influence plant productivity (e.g. Hairston et al. 1960; Menge and Sutherland 1976;
Oksanen et al. 1981), and some historical awareness that forage quality might
influence these interactions (e.g. White 1978; Lawton and McNeill 1979). Follow-
ing this has been a growing recognition that plant traits can play an important role in
mediating the interaction between plants and herbivores (e.g. Grime 1979; Coley
et al. 1985; Díaz et al. 2006), and that plants that possess traits associated with an
acquisitive strategy and high-quality litter also produce foliage that is more palat-
able than plants which have traits characteristic of a conservative strategy (Grime
et al. 1996). Coupled with this has been a growing awareness that palatable fast-
growing plants may enter a positive feedback with their herbivores which involves
enhanced soil fertility, as shown by classical studies on grasslands in the Serengeti
(McNaughton 1983, 1985). Similarly, there is also recognition that herbivory in
less productive ecosystems can lead to a negative feedback whereby palatable plant
species are replaced by less palatable species which produce poorer-quality litter,
leading to reduced soil fertility and ecosystem productivity, as shown in classical
studies involving moose (Alces alces) browsing in Isle Royale, Michigan, USA
(Pastor et al. 1988). Herbivores and their ecological effects are in turn governed by
their predators, and although historically the importance of predator-induced
trophic cascades in terrestrial ecosystems has been questioned (Strong 1992; Polis
1994), the last decade has witnessed increasing recognition that trophic cascades
in at least some terrestrial environments have a significant role in modulating
herbivore effects on plant communities and therefore upon ecosystem processes
(e.g. Pace et al. 1999; Terborgh et al. 2001)
Plant communities consist of multiple coexisting plant species, and an issue that
has long fascinated ecologists is how combinations of plant species influence eco-
system processes (Odum 1969). For instance, many early studies have explicitly
investigated how multiple species combinations and species diversity influence
ecosystem stability (McNaughton 1977), productivity (Trenbath 1974; Austin and
Austin 1980), and soil biota (Christie et al. 1974, 1978; Chapman et al. 1988).
However, from the mid-1990s, notably following publication of the book Biodiver-
sity and Ecosystem Function edited by Schulze and Mooney (1993), this field has
attracted considerable attention, and many experimental studies have been performed
since the mid-1990s to demonstrate the role of species diversity as a driver of
ecosystem processes (e.g. Naeem et al. 1994; Tilman et al. 1996; Hector et al.
1999), although the interpretation of these studies has caused much debate (Aarssen
1997; Huston 1997; Kaiser 2000; Hooper et al. 2005). Other studies have addressed
this issue from a combined aboveground–belowground perspective, either by con-
sidering how plant biodiversity influences belowground organisms and processes
(e.g. Hooper and Vitousek 1997, 1998; Wardle et al. 1997b, 1999), or how biodiver-
sity of belowground organisms affects aboveground organisms and processes (e.g.
Van der Heijden et al. 1998b; Laakso and Setälä 1999a) Many issues remain
unresolved about the importance of species diversity in driving ecosystem processes
in real (natural or non-experimental) ecosystems, as will be discussed in Chapter 5,
8 • 1 Introduction

and multiple points of view about this topic persist (e.g. Tilman 1999; Leps 2004;
Grace et al. 2007; Duffy 2009; Wardle and Jonsson 2010).

1.3 Aboveground–belowground interactions as drivers of

ecosystem processes
Traditionally, the aboveground and belowground components of ecosystems have
frequently been considered in isolation from one another. However, as noted above,
the last two decades have witnessed a proliferation of studies exploring the influence
that these components exert on each other, and the fundamental role that aboveground–
belowground interactions play in controlling the structure and functioning of terrestrial
ecosystems. As will be demonstrated throughout this book, this has led to an increased
recognition of the role that aboveground–belowground interactions play as terrestrial
ecosystem drivers, and their increasing inclusion as a fundamental element of ecosys-
tem ecology (Wardle et al. 2004a). This development has been driven in part by issues
discussed above, such the growing understanding of the roles that plant species and
litter quality play in regulating decomposition processes (e.g. Swift et al. 1979; Cadisch
and Giller 1997). However, other issues have also contributed to this development,
some of which we highlight here.
As has been documented elsewhere (e.g. Wardle 2002), the discipline of soil
science, including soil biology, has historically often given relatively little attention
to what goes on aboveground. However, in the late 1970s and early 1980s, soil
ecologists focused increasingly on the significance of trophic interactions in soil for
decomposition and nutrient-cycling processes (Coleman et al. 1977; Anderson et al.
1981; Anderson and Ineson 1984; Clarholm 1985; Coleman 1985). These trophic
interactions were shown to influence the supply of plant-available nutrients from the
soil, and subsequent studies pointed to their role in influencing plant nutrient acqui-
sition and growth. For example, the classic experimental study by Ingham et al.
(1985) showed that the addition microbial-feeding nematodes to soil enhanced
nitrogen uptake by and growth of the grass Bouteloua gracilis. Similarly, Setälä
and Huhta (1991) showed that leaf, stem, and shoot biomass of birch (Betula
pendula) seedlings was increased when they were grown in the presence of a diverse
soil fauna. These studies laid the foundation for many subsequent experiments which
have shown multitrophic interactions in soil to serve as drivers of plant nutrient
acquisition and growth (e.g. Alphei et al. 1996; Bardgett and Chan 1999; Laakso and
Setälä 1999a, 1999b; Cole et al. 2004), plant community structure (Brown and Gange
1990; Bradford et al. 2002), and consumers of plant material (e.g. Gange and Brown
1989; Scheu et al. 1999; Bonkowski et al. 2001). Moreover, as will be discussed in
Chapter 2, this research has led to the recognition that non-nutritional links also occur
between soil and plant communities through soil animals affecting bacterial produc-
tion of plant growth-promoting hormones (Jentschke et al. 1995; Alphei et al. 1996;
Bonkowski 2004). Consequently, effects of belowground communities on plant
growth are now increasingly recognized as being highly complex, and involving a
 1.3 Drivers of ecosystem processes • 9

variety of nutritional and non-nutritional responses to microbial grazing (Bonkowski

2004).
It has long been known that plant and soil communities are linked through the
actions of root-associated biota, including symbionts, parasites, pathogens, and root
herbivores. Mycorrhizal fungi, which associate with roots of some 80% of all
terrestrial plant species (Smith and Read 1997), have received a particularly large
amount of attention. An important development has been the recognition that the
major mycorrhizal types differ both in the types of ecosystem in which they dominate
and the types of function that they perform (Harley 1969; Read 1994). For example,
trees and shrubs of temperate and boreal forests and shrublands, especially those that
are nutrient-limited, are known to have an obligate need for ectomycorrhizae and
ericoid mycorrhizae, which perform a crucial role in the acquisition organic nutrients
contained in litter and humus in these ecosystems (Leake and Read 1997; Read and
Perez-Moreno 2003). Meanwhile, arbuscular mycorrhizal fungi, which dominate in
grasslands and many temperate and tropical forests, have been shown to play a
significant role in structuring plant communities. For example, in a classic study,
Grime et al. (1987) manipulated arbuscular mycorrhizal fungi in grassland micro-
cosms and found that their presence caused a reduction in dominance of competitive
grass species in favour of several subordinate herb species, in turn increasing plant
species diversity. This study laid the foundation for several other studies which have
manipulated mycorrhizal communities and revealed their role as powerful drivers of
plant community dynamics (e.g. Gange et al. 1993; Newsham et al. 1995a; Van der
Heijden et al. 1998a; Hartnett and Wilson 1999). At around that time, an increasing
number of studies began to explore the role of nitrogen-fixing symbionts as drivers of
vegetation dynamics and ecosystem functioning in natural ecosystems (e.g. Vitousek
and Walker 1989; Olff et al. 1993; Chapin et al. 1994), leading to new discoveries
about roles that they play in the nitrogen cycle of particular ecosystems. For example,
nitrogen-fixing cyanobacteria which inhabit the incurves of leaves of the feather moss
Pleurozium schreberi (the most common moss on Earth) have been found to fix
significant quantities of nitrogen in boreal forests (De Luca et al. 2002b). Also, leaf
cutter ants, which are prevalent in neotropical ecosystems, have been shown to
engage in mutualistic associations with nitrogen-fixing bacteria in their belowground
fungal gardens, leading to significant ecosystem inputs of nitrogen (Pinto-Tomás
et al. 2009).
Another topic that has contributed to the development of interest in aboveground–
belowground interactions involves the nature of feedbacks between the two subsys-
tems. One aspect that is attracting increasing attention involves the role of soil
antagonists—that is, root pathogens and herbivores—in regulating vegetation dy-
namics via negative feedback. The mechanism involved, namely the accumulation of
specific plant antagonists that inhibit the growth of the host plant, is well established
in agricultural science, and forms the basis of crop rotations for the prevention of
build up of crop-specific pathogens in soil. However, the role of these antagonists in
natural ecosystems only began to be appreciated in the last two decades through
studies pointing to their role in driving vegetation dynamics (e.g. Brown and Gange
10 • 1 Introduction

1989, 1992; Van der Putten et al. 1993; Bever 1994). These studies laid the founda-
tion for many subsequent studies, particularly in the past five years, which have
placed the concept of negative feedback firmly within the ecological literature
(Kulmatiski et al. 2008; Van der Putten 2009). Meanwhile, other studies have
plant–soil feedbacks in which plants provide resources for decomposers as plant
litter and rhizosphere materials, and the decomposers in turn release nutrients from
these materials for plant growth. These include studies which have shown plant
species to differentially influence soil biological communities (e.g. Rovira et al.
1974; Grayston et al. 1998; Bardgett et al. 1999c) and nutrient cycling in their
immediate vicinity (e.g. Northup et al. 1995; Berendse 1998), and to preferentially
select for decomposer taxa that enhance the decomposition of their own litter
(e.g. Hunt et al. 1988; Hansen 1999; Vivanco and Austin 2008; Ayres et al. 2009).
Moreover, classic studies on aboveground herbivore effects on ecosystems have
shown herbivores to alter soil fertility in a manner that can feed back to plant growth
both positively (McNaughton 1983, 1985) and negatively (Pastor et al. 1988, 1993).
Other studies have revealed that plant–soil feedbacks involving herbivory can also
operate at the individual plant level (Seastedt 1984). As such, there is growing
evidence that defoliation causes a short-term pulse of root exudates which stimulates
soil biotic activity (Holland et al. 1996; Mawdsley and Bardgett 1997), leading to
increased soil nitrogen mineralization and plant nitrogen acquisition, and ultimately
benefiting plant growth (Hamilton and Frank 2001).

1.4 Aboveground–belowground interactions

and global change
Human activities have a substantial and ever-growing impact on ecosystems, to the
extent that much of the Earth’s land surface has been transformed by a suite of global-
change phenomena (Vitousek et al. 1997c). The most obvious human impact on Earth
is through the increasing transformation of land for food production and forestry,
which is presently the primary driving force behind the loss of biological diversity on
both local and global scales (Sala et al. 2000; Millennium Ecosystem Assessment
2005). However, every terrestrial ecosystem on Earth is also simultaneously affected
by a suite of other global change phenomena and their interactions, including global
climate change, the invasion of alien species into new territories, losses of existing
species, and increasing rates of nitrogen deposition. The last two decades have
witnessed a vast number of studies exploring the impacts of these global change
phenomena on the structure and functioning of terrestrial ecosystems. Concomitant
with this has been a developing awareness that understanding the consequences of
global phenomena requires explicit consideration of linkages between aboveground
and belowground biota (e.g. Wardle et al. 1998c; Wolters et al. 2000). This is
because, with the exception of disturbances that directly impact on belowground
biota and the processes that they drive, the influence of global change phenomena on
terrestrial ecosystems is largely indirect via changes that occur aboveground. These
 1.4 Global change • 11

include shifts in plant community composition, spectra of plant traits, carbon-

allocation patterns, and the quantity and quality of plant-derived organic matter
entering soil. In turn, such belowground responses to global change, both direct
and indirect, create feedbacks that affect aboveground biota, ecosystem nutrient and
carbon dynamics, and the flux of carbon dioxide and other greenhouse gases from
land to the air.
The driver of global change that has perhaps attracted the most attention in this
context is climate change. As such, a number of studies have contributed to the now
widespread recognition that an understanding of the impacts of climate change on
terrestrial ecosystems and Earth-system feedbacks requires explicit consideration of
belowground biota and their linkages aboveground (Bardgett et al. 2008; Tylianakis
et al. 2008). For instance, several studies in the 1990s revealed that elevated concen-
trations of carbon dioxide in the atmosphere can indirectly impact on soil organisms
through changing the quantity and quality of plant litter returned to soil, the rate of
root turnover, and the exudation of carbon from roots into soil (Billes et al. 1993;
Jones et al. 1998; Coûteaux et al. 1999). These effects on soil biota were also found to
have important consequences for the dynamics of nutrients in soil and hence their
availability to plants, thereby enforcing either positive or negative interactions with
plant growth depending on context (Zak et al. 1993; Díaz et al. 1993). Another area
that has attracted much attention concerns the effects of climate warming on organic
matter decomposition in soil. Of particular relevance is the pioneering work of
Jenkinson et al. (1991), who demonstrated that rising temperatures could accelerate
rates of soil microbial respiration, thereby increasing the transfer of carbon dioxide to
the atmosphere and promoting a positive feedback on climate change. Although this
study was primarily concerned with a direct effect of climate warming on the activity
of heterotrophic microbes, subsequent work has shown the temperature dependence
of decomposition to vary with organic matter quality (e.g. Luo et al. 2001; Melillo
et al. 2002; Fierer et al. 2005), and thus the quality of plant material entering the soil.
Human activities have also lead to major increases in global emissions of nitrogen
to the atmosphere, leading to dramatic increases in the deposition of atmospheric
nitrogen to the terrestrial biosphere (Holland et al. 1999; Bobbink and Lamers 2002;
Galloway et al. 2004). As with climate change, it is now well known that
such nitrogen enrichment can greatly modify terrestrial ecosystems by affecting
aboveground–belowground feedbacks. As will be discussed in Chapter 2, a signifi-
cant body of literature has developed showing that effects of nitrogen enrichment can
directly impact on belowground organisms (e.g. Scheu and Schaefer 1998; Donnison
et al. 2000; Egerton-Warburton and Allen 2000) and extracellular enzymes involved
in decomposition processes (e.g. Carreiro et al. 2000; Frey et al. 2004). However, as
will be discussed in Chapter 3, a growing number of studies have also suggested that
impacts of nitrogen enrichment may be indirect, by altering the composition of the
plant community (Bobbink 1991; Bowman et al. 1993; Wedin and Tilman 1993),
although explicit tests of this are still scarce (e.g. Manning et al. 2006, Suding et al.
2008). Another important development in this area is the recognition that interactive
effects on the belowground subsystem of nitrogen enrichment and climate change
12 • 1 Introduction

have the potential to strongly influence ecosystem functioning. For instance, it is now
widely recognized that the response of terrestrial ecosystems to elevated carbon
dioxide concentrations is limited by nitrogen availability (e.g. Luo et al. 2004) and
that nitrogen enrichment can amplify climate-change-driven changes in vegetation
composition, thereby increasing the potential for indirect effects of vegetation change
on the belowground subsystem (Wookey et al. 2009). Also, as we will discuss in
Chapter 2, nitrogen deposition can have substantial effects on decomposition pro-
cesses, thereby influencing the response of soil respiration to warming and the
capacity of soils to sequester carbon under climate change (Davidson and Janssens
2006; Bardgett et al. 2008).
Another element of human-driven global change that has attracted much recent
attention is how invasion of alien species into new territories affect ecosystem
properties. For instance, a body of literature has been developing for over 20 years,
which includes the classic studies of Vitousek et al. (1987) and Vitousek and Walker
(1989) described above, revealing that invasion of alien plants into new territories
can have strong effects both aboveground and belowground, when the invading
species has vastly different physiological traits from the native flora. As described
in Chapter 5, there is now much evidence showing that invasive plants may greatly
affect the quantity and quality of resource inputs to decomposer organisms and the
processes that they drive, ultimately affecting soil nutrient availability (Ehrenfeld
2003; Liao et al. 2008). Further, starting with the work of Klironomos (2002), several
recent studies have also focused on aboveground–belowground feedbacks which
operate via interactions between invasive species and root-associated biota,
for example in terms of escape of the invader from natural soil-borne enemies
(e.g. Reinhart et al. 2003; Callaway et al. 2004). Moreover, as will be discussed in
Chapter 5, a handful of studies over the past decade have shown major transform-
ations by invasive animals of both the aboveground and belowground components of
ecosystems; some of the most spectacular examples involve invasive herbivores such
as moths (Lovett et al. 2006), deer (e.g. Wardle et al. 2001; Vázquez 2002), and
beavers (Castor canadensis) (Anderson et al. 2006), and cascading effects of invasive
predators such as rats (Rattus spp.) (Fukami et al. 2006), foxes (Croll et al. 2005), and
ants (O’Dowd et al. 2003). Finally, as will also be highlighted in Chapter 5, recent
evidence suggests that range-expanding species under climate change can have
important effects on ecosystem properties and, potentially, carbon-cycle feedbacks
by affecting aboveground–belowground feedbacks (e.g. Knapp et al. 2008; Kurz
et al. 2008), and that belowground biota might play a role in affecting range
expansion of species under climate change (Engelkes et al. 2008).

1.5 Emerging issues and trends

As highlighted throughout this chapter, aboveground–belowground interactions and
feedbacks are highly complex and operate at a wide range of temporal and spatial
scales. Despite the rapid development of this field, many challenges remain, as we
 1.5 Emerging issues and trends • 13

will highlight in this book. Perhaps one of the most significant challenges, however,
is the need for a stronger theoretical basis for the subject, in that almost all studies on
aboveground–belowground interactions have been carried out from an empirical
perspective and modelling approaches are still in their infancy (Van der Putten
et al. 2009). As a consequence, our ability to make predictions about the role of
aboveground–belowground interactions and feedbacks in regulating terrestrial
ecosystem processes and their response to global change remains limited. A related
issue that is emerging is the need to demonstrate the significance of aboveground–
belowground interactions as drivers of community dynamics and functioning of real
ecosystems, and the importance of their role relative to that of abiotic factors. As will
be discussed in Chapter 5, this point is especially relevant for understanding the
importance of consequences of species loss (and gain) for the functioning of real
terrestrial ecosystems, and stems partly from the fact that relatively few studies have
considered the impacts of non-random species losses in real ecosystems and how they
vary in different environment contexts. As we argue in Chapter 5, the most product-
ive way forward here would be the widespread use of experimental or theoretical
approaches that directly investigate how loss of species, such as may result from
global environmental change, directly impacts upon other organisms and ecosystem
processes in real ecosystems.
Another emerging issue that we consider throughout this book concerns soil-
carbon dynamics and especially the role that soils play in the global carbon cycle
and climate change. This interest has arisen because soils absorb and release green-
house gases (notably carbon dioxide and methane), and act as a major global carbon
reservoir, storing some 80% of the Earth’s terrestrial carbon stock (IPCC 2007).
Despite the importance of soils for carbon cycling, remarkably little is known about
the factors that regulate the fluxes of carbon to and from soil, or about the role that
interactions between plants and soil biota play in regulating soil-carbon cycling
(Wardle et al. 2004a; Bardgett et al. 2009; Peltzer et al. 2010). The last few years
have witnessed a proliferation of studies into the ecological and biogeochemical
dynamics of carbon-cycling processes in soils, including investigations into plant
and rhizosphere effects on soil respiration, effects of soil microbial communities on
plant productivity and soil-carbon turnover, and interactions among element cycles
(e.g. carbon, nitrogen, and phosphorus). However, current models of the global
carbon cycle seldom include these processes; rather, they simply treat net carbon
emissions from ecosystems as the balance between net primary production (NPP) and
heterotrophic respiration. An emerging challenge is therefore to use our advancing
understanding of plant and soil microbial processes involved in carbon cycling to
improve the representation of aboveground–belowground interactions in carbon-
cycle models.
Finally, an issue that has attracted much attention in recent years is the value of
ecosystems in providing ecosystem goods and services, or the benefits that people
derive from ecosystems (Ehrlich and Mooney 1983; Tscharntke et al. 2005; Hooper
et al. 2005). These benefits are obvious and wide-ranging, and include carbon
sequestration, climate regulation, the provision of clean water, and the maintenance
14 • 1 Introduction

of soil fertility and primary production (food, fodder, and fibre). This issue has moved
the science of ecosystem ecology beyond the scientific community to the global
policy community, as politicians increasingly recognize ecosystems as natural capital
assets that supply life-support services of great value (Daily and Matson 2008).
A major impetus for this change was the publication of the Millennium Ecosystem
Assessment (2005), which presented a new conceptual framework for documenting,
analysing, and understanding the effects of global change on ecosystems and human
well-being, viewing ecosystems in terms of the services that they provide for society.
This approach has been adopted widely among the scientific and policy communities
and has led to new approaches for research, conservation, and sustainable develop-
ment (Carpenter et al. 2009; Daily and Matson 2009). Moreover, this approach
presents many new challenges for ecosystem ecologists, most notably the need to
understand biotic drivers of ecosystems, including aboveground–belowground inter-
actions, in the context of ecosystem services and human well-being. As noted by
Carpenter et al. (2009), this requires a new kind of interdisciplinary science that
considers the interactions of social and ecological constituents of the Earth-system.
While the issue of ecosystem service provision is not a primary focus of this book,
our synthesis does provide a basis for understanding the biotic factors that influence
their provision and how this provision may be driven by aboveground–belowground
linkages and their responses to global change.
2
Biotic interactions in soil as drivers of
ecosystem properties

2.1 Introduction
It has long been appreciated that soil organisms are central to the maintenance of soil
fertility and the functioning of terrestrial ecosystems. For example, the pioneering
work of Winogradsky (1856–1953) established some of the fundamental roles that
soil microbes play in the nitrogen and sulphur cycles, and in 1881 Darwin published
his last book, The Formation of Vegetable Mould through the Action of Worms and
Observations on their Habits, which recognized the important roles that earthworms
perform in biogeochemical cycles. Despite this historical recognition of the contri-
bution of soil organisms to soil fertility, it is only in recent years that community and
ecosystem ecologists have more fully recognized the key role that belowground
organisms and biotic interactions play in determining a range of important ecosystem
processes, including decomposition, nutrient and carbon cycling, and soil formation.
Moreover, it has only relatively recently been recognized that the soil biological
community represents a major, but largely unexplored, reservoir of global biodiver-
sity (Whitman et al. 1998; Torsvik et al. 2002; Bardgett 2005). For instance, it has
been estimated that 1 g of soil can contain up to 50 000 bacterial species (Curtis et al.
2002; Torsvik et al. 2002), and up to 200 m of fungal hyphae (Read 1992; Bardgett
et al. 1993a). Further, as many as 89 nematode species have been found in a single
soil core in Cameroon tropical forest (Bloemers et al. 1997) and 159 mite species
were identified in a patch of prairie grassland soil in Kansas (St John et al. 2006).
Recently, the analysis of soil DNA by Wu et al. (2009) revealed an estimated 1320
and 2010 operational taxonomic units (OTUs) of fauna in Alaskan boreal forest and
tundra, respectively. Despite this growing recognition of both the diversity and
functional importance of soil organisms for ecosystem processes, our understanding
of the impact of soil biotic interactions on community and ecosystem properties is
still in its infancy.
As noted in Chapter 1, the last decade has seen a dramatic increase in the number of
studies showing that aboveground and belowground communities are intimately
linked, and that feedbacks between the aboveground and belowground subsystems
play fundamental roles in controlling ecosystem processes and properties (e.g.
Hooper et al. 2000; Van der Putten et al. 2001, 2009; Scheu and Setälä 2002; Wardle
2002; Wardle et al. 2004a; Bardgett et al. 2005; Van der Heijden et al. 2008). The
16 • 2 Biotic interactions as ecosystem drivers

complexity of possible interactions between aboveground and belowground commu-

nities, and hence their consequences for ecosystem properties, is enormous (Wardle
2002; Wardle et al. 2004a; Van der Heijden et al. 2008). However, as a general
framework (Fig. 2.1), plants regulate the quantity and quality of resources available
for the functioning of the decomposer community and for obligate belowground
biotrophs, such as root herbivores, pathogens, and symbiotic mutualists. In turn, the
belowground community regulates plant growth and community composition indir-
ectly through the activity of the decomposer food web (which regulates the supply of
available soil nutrients to plants), and directly through the action of root-associated
biotrophs (Wardle et al. 2004a). In this way, biotic interactions between aboveground

b2 b1
c2 c1

Detritus food
Pathogens web

Mycorrhizae

Root-feeding
fauna

Direct pathway to plants Indirect pathway to plants

Fig. 2.1 Schematic diagram showing interactions of aboveground communities with soil food-
web organisms. On the right-hand side, the feeding activities in the detritus food web (solid
arrows) stimulate nutrient turnover (large grey arrow), plant nutrient acquisition (a), plant
performance, and thereby indirectly influence aboveground herbivores (broken arrows) (b1).
On the left-hand side, soil biota exert direct effects on plants by feeding upon roots and forming
antagonistic or mutualistic relationships with their host plants. Such direct interactions with
plants influence not just the performance of the host plants themselves, but also that of the
herbivores (b2) and ultimately their predators. Further, the soil food web can control the
successional development of plant communities both directly (c2) and indirectly (c1), and
these plant community changes can in turn influence soil biota. From Wardle et al. (2004a),
with permission from the American Association for the Advancement of Science.
 2.2 Influence of decomposers • 17

and belowground communities act as powerful drivers of community and ecosystem

properties, and play an important role in regulating the response of terrestrial eco-
systems to human-induced global change.
In this chapter, we explore one part of this feedback, namely how interactions
between the vast diversity of organisms that live in soil regulate important ecosystem
processes, and how they indirectly and directly influence the productivity, diversity,
and composition of plant communities. The other component of this feedback,
namely how plants in turn affect those organisms that inhabit the soil, is considered
in Chapter 3. First, we describe the roles that the soil biological community play in
regulating ecosystem processes and the productivity and composition of plant com-
munities through their influence on the mineralization of nutrients. Second, we
explore how root-associated organisms affect plant productivity and community
structure, including their role in driving succession and invasion. Third, we examine
how belowground engineers modify soil nutrient dynamics and plant communities
through altering the physical environment in the soil. Finally, we discuss the role of
soil biotic interactions in a global change context, focussing on their influence on
ecosystem carbon dynamics and contribution to climate change via carbon-cycle
feedbacks. The ultimate aim of this chapter is to highlight the significance of soil
biotic interactions for ecosystem processes, the productivity and diversity of plant
communities, and carbon and nutrient dynamics under global change.

2.2 Influence of decomposers on aboveground

communities and ecosystem processes
Ecosystem ecologists have long recognized the importance of dead organic matter, or
detritus, for community organization and ecosystem energy flow (Odum 1969; Swift
et al. 1979; Moore et al. 2004). As such, it is well established that detritus provides
both a resource and habitat for the various components of the decomposer food web,
including microbial decomposers, detritivores, microbivorous organisms, and pred-
ators (Wardle 2002; Moore et al. 2004) (Fig. 2.2). In turn, the decomposer commu-
nity strongly influences aboveground community organization and ecosystem
processes through its role in the breakdown and transformation of organic matter,
and liberation of plant growth-limiting nutrients (Fig. 2.2). In this section, we
demonstrate the various mechanisms by which biotic interactions within the decom-
poser food web influence plant communities indirectly through their affect on
decomposition processes and nutrient dynamics.

2.2.1 Free-living soil microbes, nutrient availability, and plant growth

Plant growth is primarily limited by the availability of nutrients (Vitousek 2004), and
hence any biotic interaction in soil that alters the rate and timing of nutrient supply
to plants (whether positive or negative) will influence plant growth and potentially
plant community dynamics. Biotic interactions that occur in the rhizosphere are of
18 • 2 Biotic interactions as ecosystem drivers

Carnivores

Detritivores/microbivores

Herbivores Decomposers

Plants Detritus

Soluble nutrients

Allochthonous Allochthonous
inputs inputs

Fig. 2.2 Features of a generalized food web incorporating detrital dynamics, including
resource inputs into the web and internal cycling within the web. The solid black arrows
represent the flow of matter through the grazer pathway that originates from primary producers,
whereas the broken black arrows represent the decomposer pathway that originates from
detritus (external imports and internal pools). The solid grey arrows depict the autochthonous
flow of matter to the detritus pool that results from death of all living organisms and from
unassimilated prey. The broken grey arrows signify the mineralization and immobilization of
soluble nutrients. From Moore et al. (2004), with permission from Wiley-Blackwell.

importance for plant nutrient supply, as this is the zone of soil that is most strongly
influenced by plant roots and their exudates (Bardgett 2005). Here, microbial processes
of nutrient mineralization occur whereby soluble and insoluble organic matter is broken
down and converted to inorganic plant available forms, strongly regulating plant
nutrient supply (Kaye and Hart 1997; Jones et al. 2005; Schimel and Bennett 2004).
Most soil nitrogen (96–98%) is contained in dead organic matter as complex
insoluble polymers such as proteins, nucleic acids, and chitin. These polymers are
broken down into dissolved organic nitrogen by extracellular enzymes produced by
soil microbes (Schimel and Bennett 2004). This dissolved organic nitrogen can
constitute a significant portion of the total soluble nitrogen pool (Jones and Kielland
2002) and can be absorbed by free-living soil microbes, mineralized by the microbial
biomass (i.e. converted from an organic to inorganic form, with inorganic nitrogen
being liberated into the soil environment), or taken up directly by plant roots in the
form of amino acids and bypassing the microbial mineralization step. Direct uptake of
amino acids by plants appears to be especially important in strongly nitrogen-limited
ecosystems, such as in Arctic and alpine tundra (Raab et al. 1999; Nordin et al. 2004),
 2.2 Influence of decomposers • 19

boreal (Näsholm et al. 1998; Nordin et al. 2001) and temperate forest (Finzi and
Berthrong 2005), and low-fertility grasslands (Bardgett et al. 2003; Weigelt et al.
2005; Harrison et al. 2007). Recent recognition of the importance of direct uptake by
plants has led to a radical rethink of terrestrial nitrogen cycling and of the processes
that control plant N availability (Schimel and Bennett 2004; Jones et al. 2005). In a
similar way, microbes also influence the mineralization of organic phosphorus
through the production of phosphatases, which cleave ester bonds in organic matter
and liberate inorganic phosphorus for plant uptake. Unlike nitrogen, most reactions
that govern phosphorus availability to plants are geochemical rather than biological,
although, as will be discussed later in this chapter, mycorrhizal fungi play an
important role in the uptake of phosphorus by plants.
Microbes in soil also compete with plants for nutrients in soil solution, with
potentially negative effects on plant nutrient acquisition and growth. This is most
likely to occur in strongly nutrient-limited ecosystems such as Arctic and alpine
tundra (Schimel and Chapin 1996; Nordin et al. 2004). Further soil microbes have
been shown to compete effectively with plants for nitrogen in nutrient-poor grass-
lands (Bardgett et al. 2003; Harrison et al. 2007), and this can lead to as much
nitrogen being stored in the microbial pool as in the plant pool (Jonasson et al. 1999;
Bardgett et al. 2007b). However, in some ecosystems, soil microbes are not a
significant sink for nitrogen, especially when the availability of mineral nitrogen
and rates of nitrification are high. For instance, 15N-tracer studies in tropical humid
forests reveal that those ecosystems which typically lack nitrogen limitation are
characterized by very rapid rates of nitrification and negligible microbial assimilation
of nitrogen (Silver et al. 2001, 2005; Templer et al. 2008), especially when concen-
trations of mineral nitrogen in soil are high (Vitousek and Matson 1988). Similarly,
15
N-tracer studies in temperate grasslands in England reveal that microbial nitrogen
uptake and retention is substantially less in high-fertility (e.g. fertilized) grassland
where rates of nitrogen mineralization and nitrification are relatively high, than in
low-fertility grassland with low rates of nitrogen turnover (Bardgett et al. 2003).
Collectively, these studies point to the microbial community acting as greater nitro-
gen sink in nitrogen-limited ecosystems than in nitrogen-rich ecosystems. Moreover,
they indicate the different roles that soil microbes play in nitrogen retention and loss:
microbial nitrogen uptake appears to play a significant role in ecosystems where
nitrogen limits plant growth (Jackson et al. 1989; Fisk et al. 2002; Zogg et al. 2000;
Bardgett et al. 2003), whereas nitrification plays a key role in ecosystems that are
nitrogen replete (Silver et al. 2001, 2005; Templer et al. 2008).
Plants and soil microbes compete for soil nitrogen (Kaye and Hart 1997; Dunn
et al. 2006), through close linkages that occur in the rhizosphere (Frank and Groffman
2009). However, they can also avoid competition through partitioning of the ecosys-
tem nitrogen pool over seasons (Jaeger et al. 1999; Bardgett et al. 2005). In particular,
studies in alpine regions reveal the existence of a strong link between the temporal
dynamics of microbial communities and plant nutrient supply. Here, as in other
seasonal ecosystems, it has traditionally been assumed that soil microbes are inactive
during the winter. However, it has recently been shown that the biomass of microbes
20 • 2 Biotic interactions as ecosystem drivers

in alpine soils is maximal during late winter when the soil is frozen (Schadt et al.
2003), and that seasonal changes in microbial biomass are associated with shifts in
microbial community composition (Lipson and Schmidt 2004). Specifically, fungi
that utilize complex plant residues dominate in the winter, whereas bacteria that
thrive on root exudates are more active in the summer (Lipson and Schmidt 2004).
Moreover, there is an almost complete turnover of the microbial community between
winter and summer, with a large number of novel DNA sequences (Schadt et al. 2003)
associated with specific functional attributes occurring only in the winter or only in the
summer (Lipson and Schmidt 2004). These seasonal dynamics in microbial commu-
nities are of importance because they control the temporal partitioning of nitrogen
between plants and soil microbes over seasons. For example, in an alpine meadow in
Colorado, Jaeger et al. (1999) found that the dominant plant species Kobresia myo-
suroides took up nitrogen maximally after snowmelt, whereas the soil microbial
community immobilized nitrogen maximally in the autumn following plant senes-
cence, and then retained this nitrogen throughout the winter. The release of microbial
nitrogen for plant uptake in spring appears to be facilitated by a decline in microbial
biomass after snowmelt, leading to a pulse of soluble nitrogen in the form of protein
into soil (Lipson and Schmidt 2004). This pulse coincides with a peak in soil protease
activity, which facilitates the supply of amino acids for plant uptake at a time of high
plant nitrogen demand (Raab et al. 1999). Together, these studies indicate that in
nitrogen-limited ecosystems the cycling of labile nitrogen pools over seasons relies on
intimate, temporal coupling between plants and microbes and their seasonal resource
demands (Fig. 2.3) (Bardgett et al. 2005; Frank and Groffman 2009).
Free-living microbes can also influence plant community dynamics through alter-
ing the availability of different chemical forms of nitrogen for plant uptake. The
proposed mechanism here is that coexisting plant species partition a limited nitrogen
pool (thereby avoiding competition for nitrogen), through the uptake of different
chemical forms of soil nitrogen which have been produced by microbial enzymes
and mineralization processes. Two lines of evidence support for this idea. First, it is
known that microbial activities produce a wide variety of nitrogen forms in soil
solution, including inorganic nitrogen forms and a variety of amino acids of varying
complexity (Kielland 1994), which provides a variety of possible resources for plant
uptake. Second, several studies show that plant species are highly versatile in their
ability to uptake different chemical forms of nitrogen (Weigelt et al. 2005; Harrison
et al. 2007, 2008), and that species differ in their ability to uptake nitrogen forms,
pointing to them having niches based on nitrogen form (Miller and Bowman 2002,
2003; Weigelt et al. 2005; Harrison et al. 2008). Moreover, coexisting species of
nitrogen limited Arctic tundra plants have been shown to differ in the chemical forms
of nitrogen that they take up, with the dominant plant species using the most abundant
nitrogen form that is present in soil (McKane et al. 2002). This is indicative of species
niche partitioning based on the chemical form of nitrogen (McKane et al. 2002).
Meanwhile, 15N-labelling studies of low-fertility grasslands in Germany show that
different plant functional groups rely on different nitrogen pools to meet their nitrogen
demands, also suggesting that nitrogen-uptake patterns across functional groups are
 Litter C inputs (more recalcitrant compounds)

Snow cover

= fungal population
= bacterial population

Winter phase

Litter C inputs

N CO2
Flush of N N CO2

= fungal population = fungal population

= bacterial population = bacterial population

Spring phase Autumn phase

High fine High C

root turnover root exudation

N N

= fungal population
= bacterial population

Summer phase

Fig. 2.3 Seasonal dynamics of plant and microbial resource demands in strongly nitrogen-limited alpine ecosystems. In autumn, senescing plants
provide a pulse of labile carbon to support microbial growth, and in winter the microbial biomass, and especially fungi which degrade recalcitrant
polyphenolic compounds, continues to increase as carbon and nitrogen in plant litter is consumed and mineralized by the microbial community. In spring,
rapid changes in microclimate and the exhaustion of labile carbon compounds lead to enhanced turnover of microbial community, with concomitant
release of labile N for plant uptake, and in summer plant uptake of nitrogen continues to meet growth demands, followed by a period of C sequestration
and loss to soil microbes. From Bardgett et al. (2005), with permission from Elsevier.
22 • 2 Biotic interactions as ecosystem drivers

driven by different niches based on the chemical form of nitrogen (Kahmen et al.
2006) (Fig. 2.4). A similar idea has been proposed for partitioning of the soil
phosphorus pool: a large number of biologically available phosphorus compounds
occur in soil and there are likely to be a variety of mechanisms, some involving soil
microbes, through which plants can access them (Bardgett 2005; Turner 2008). This is
thought to occur widely in terrestrial environments, but especially where productivity
is limited by the availability of soil phosphorus, such as in humid temperate regions
and ecosystems developed on strongly weathered soils (Turner 2008).
Although it is tempting to conclude that partitioning on the basis of chemical form
might provide a mechanism for plants to efficiently partition a limited soil nutrient
pool, thereby facilitating species coexistence and the maintenance of plant diversity
(McKane et al. 2002; Reynolds et al. 2003; Kahmen et al. 2006), not all studies
support this idea. A recent field-based 15N-labelling study in relatively fertile tem-
perate grassland by Harrison et al. (2007) found that while coexisting plant species
varied markedly in uptake rates of different chemical forms of nitrogen, they all
preferentially took up 15N-labelled inorganic nitrogen over more complex amino
acids, and more simple amino acids over complex ones. It has been proposed that
variation in the capacity of plant communities to uptake and partition the nitrogen
pool based on chemical form is related to the shifting dominance of nitrogen forms
along gradients of soil fertility and ecosystem productivity, which is driven primarily

N2

Arginine
Glycine

Serine

Proteins Amino acids Ammonium Nitrate

Dead organic matter

Heterotrophic nitrification

Fig. 2.4 Individual plant species access different chemical forms of nitrogen enabling species
to coexist in terrestrial ecosystems. From Bardgett 2005, with permission from Oxford
University Press.
 2.2 Influence of decomposers • 23

by the rate of microbial turnover of components of dissolved organic nitrogen. This

idea has been proposed by a number of authors (Schimel and Bennett 2004; Jones
et al. 2005; Harrison et al. 2007), but as far as we are aware remains untested.
As discussed above, microbes can influence ecosystem nitrogen availability and
hence plant productivity by rapid transformation of nitrogen to more mobile forms,
such as nitrate through the bacterial process of nitrification, and through denitrifica-
tion whereby nitrate is lost to the atmosphere as nitrogen gases under anaerobic
conditions. Both these microbial processes cause net loss of nitrogen from soil,
especially in ecosystems such as humid tropical forests and fertilized agricultural
systems with high mineral nitrogen availability. In these systems, hydrologic
throughput and fluctuating redox conditions stimulate nitrate loss through leaching
and provide conditions optimal for denitrification (Schellekens et al. 2004; Silver
et al. 2005; Houlton et al. 2006). The impact of denitrification on plant productivity
and community composition is poorly understood, although worldwide an estimated
109–124 megatonnes of nitrogen are lost from the land surface yearly through
denitrification (Galloway et al. 2004; Seitzinger et al. 2006; Schlesinger 2009),
which may impair total global terrestrial productivity by around 7% (Schlesinger
1997). Another important recent development in this area is the discovery that
archaeal ammonium oxidizers (which perform the first step in the process of nitrifi-
cation that was previously thought to be carried out exclusively by bacteria) are the
most abundant ammonium oxidizers in soil, and are therefore likely to play a
substantial role in the nitrogen cycle (Leininger et al. 2006).

2.2.2 Trophic interactions in soil, nutrient availability, and plant growth

Plant nutrient availability is strongly regulated by microbial activities. However,
it is important to recognize that the soil also hosts an abundant and highly
complex community of invertebrates, including nematodes, collembolans, mites,
and enchytraeids, which derive most of their nutrition and carbon directly from
roots and exudates, or indirectly from feeding on the microbes that live in the root
zone (Pollierer et al. 2007). These faunal consumers of microbes, and their predators,
strongly regulate nutrient and plant community dynamics by altering the balance
between microbial immobilization and mineralization, and hence the availability of
nutrients for uptake by plants. An understanding of how belowground communities
influence aboveground community properties therefore requires explicit consider-
ation of the role of predation as a control point in the rhizosphere (Moore et al. 2003).
As mentioned above, microbes can immobilize significant quantities of nitrogen
and phosphorus, and thereby render these nutrients temporally unavailable for plant
use. For example, in strongly nutrient-limited ecosystems such as Arctic and alpine
tundra, the microbial biomass can contain up to 10% of the total ecosystem nitrogen
pool (Jonasson et al. 1999; Bardgett et al. 2002, 2007b) and 30% of the total soil
organic phosphorus pool (Jonasson et al. 1999), although as discussed above these
quantities show considerable seasonal variation. Nutrient liberation from the micro-
bial biomass can result from environmental factors, such as dry/wet or freeze/thaw
24 • 2 Biotic interactions as ecosystem drivers

cycles, which subject microbes to physiological stress (Groffman et al. 2001; Schimel
et al. 2007; Gordon et al. 2008). However, a primary mechanism by which nutrients
are liberated from microbes and made locally available for uptake by plants is through
predation of microbes by protozoa, nematodes, and microarthropods, which excrete
nutrients that are in excess of their own requirements into the soil environment and in
forms that are biologically available. This remobilization of nutrients is termed the
‘microbial loop’ (Clarholm 1985) and is considered to be a primary control point of
nutrient availability in the rhizosphere according to the nutrient-enrichment model of
Moore et al. (2003). In this model, which is based on a simple relationship between
trophic structures and detritus input (Fig. 2.5) (Moore and de Ruiter 2000), root
exudates stimulate microbial populations in the rhizosphere, in turn prompting an
increase in consumers and their predators. This increase in predation in turn leads to
increased N availability in the root zone, and enhanced plant growth due to excretion
of excess N by consumers. These changes in turn stimulate microbial growth and
turnover, which further promotes more consumers and attracts more predators
(Moore et al. 2003). Hence, nutrient availability to plants can be controlled several
trophic steps away from root through top-down control.

Phytophagous Collembolans
nematodes Predaceous
Cryptostigmatic mites
mites
Roots
Noncrypto- Predaceous
Saprophytic stigmatic mites collembolans
fungi
Fungivorous Nematode-
nematodes feeding mites
Resistant
Predaceous
nematodes
Bacteriophagous
Detritus nematodes
Flagellates
Labile Amoebae

Bacteria Bacteriophagous
mites
Inorganic
nitrogen

Fig. 2.5 Schematic of the belowground food web from the shortgrass steppe of Colorado
(Hunt et al. 1987). Species are aggregated into functional groups based on food choice and life-
history parameters. Material flows (carbon and nitrogen) are represented by solid arrows, and
net nitrogen flows are represented by dashed arrows. Plant roots, through the rhizodeposition of
labile carbon exudates and the turnover of root cells and hairs rich in resistant cell walls, initiate
the dominant materials flows in the rhizosphere. Material flows to the detritus pools and the
inorganic nitrogen pool, for example through the death rates and the excretion of waste
products, are represented as a single flow at the base of the diagram. From Moore et al.
(2003), with permission from the Ecological Society of America.
 2.2 Influence of decomposers • 25

Several experimental studies provide support for this concept, through reporting
positive effects of microbial predation by soil fauna on nutrient availability and uptake
by plants (Anderson et al. 1983; Clarholm 1985; Ingham et al. 1985; Bardgett and Chan
1999), and on plant growth (Ingham et al. 1985; Setälä and Huhta 1991; Setälä 1995;
but see Bardgett and Chan 1999). Also, it has been shown that grazing activities of soil
animals, which can be highly selective as in the case of fungal-feeding microarthopods
(Moore et al. 1985; Newell 1984a; Bardgett et al. 1993b), can lead to significant
changes in the composition, biomass, and activity of their microbial communities.
This can in turn have both positive and negative consequences for decomposition
processes and nutrient availability in soil (Mikola et al. 2002; Cole et al. 2006), although
a recent meta-analysis of litter-bag studies suggests that negative effects may be more
common, at least for microarthropods (Kampichler and Bruckner 2009). However, non-
nutritional effects of predation on plant growth can also occur, for example through
animals affecting bacterial production of plant growth-promoting hormones (Jentschke
et al. 1995; Alphei et al. 1996; Bonkowski 2004). Therefore, effects of predation on
plant growth are likely to be highly complex, and involve a combination of nutritional
and non-nutritional responses to microbial grazing (Bonkowski 2004).
Most studies on effects of soil fauna on soil processes and plants have focused on
specific interactions between particular animal taxa and microbes, mostly in very
simple microcosm systems. In nature, however, soil food webs consist of multiple
assemblages of species of several trophic groups. For this reason, multitrophic
interactions in soil have the potential to serve as a control of nutrient cycling and
plant growth. Relatively few studies have examined effects of varying the complex-
ity of soil communities on plant growth, although Bradford et al. (2002) showed that
the manipulation of soil fauna on the basis of body size in a model grassland
ecosystem brought about changes in the composition of the plant community.
When soil macrofauna were present, significant changes were detected in microbial
biomass and organic-matter decomposition, resulting in altered nutrient dynamics
and an increase in the abundance of grasses relative to herbs (Bradford et al. 2002).
In another study, Alphei et al. (1996) found that protists and nematodes enhanced
plant production, whereas earthworms reduced production. Furthermore, the posi-
tive effect of protists on plant productivity only occurred when earthworms were
absent, which is consistent with the finding of Bradford et al. (2002) that
the presence of larger-bodied soil organisms reduced the aboveground effects of
smaller-sized soil organisms.
Other studies have considered effects of the complexity of soil communities on
nutrient mineralization and plant growth in the context of diversity effects. Of note is
the classic study of Laakso and Setälä (1999a) who manipulated soil faunal commu-
nities on the basis of trophic group structure and species richness within trophic groups
to examine effects on nutrient mineralization and plant growth. They found that
variation in species composition within trophic groups was far less important for
nutrient mineralization and plant growth than was variation across trophic groups.
Further, they found that certain species, namely the enchytraeid worm Congettia
sphagnetorum, had a functionally disproportionate role in these processes. These
findings, together with those of more recent microcosm studies of the effects of animal
26 • 2 Biotic interactions as ecosystem drivers

diversity on plant nutrient uptake and growth (e.g. Cole et al. 2004), support the notion
that the effects of animal communities on plant growth are context-dependent and are
driven by the presence or absence of certain functionally irreplaceable organisms.
Modelling studies have also explored linkages between complex soil food webs and
pathways of nutrient cycling, such as the pioneering soil food-web model of Hunt et al.
(1987) of shortgrass steppe in North America. This model is based on functional
groupings of soil organisms (Fig. 2.5) and enables calculation of carbon and nitrogen
fluxes and rates of nitrogen mineralization, based on estimates of various parameters
such as the carbon-to-nitrogen ratio, rate of turnover, assimilation and production
efficiency, and population size (Hunt et al. 1987; Moore et al. 1988). This modelling
approach to the functional classification of the soil food web has been used to examine
functional responses of shifts in food-web energy channels (de Ruiter et al. 1995) and
the loss of functional groups and their combinations within soil food webs. For
example, Hunt and Wall (2002) used a simulation model based on a short-grass prairie
to show that the loss of individual functional groups of soil organisms had little effect
on nitrogen mineralization and plant production, due largely to compensatory re-
sponses in the abundances of remaining functional groups.

2.2.3 Functional consequences of trophic cascades in the soil food web

Most of the above examples of predation focus on consumers of microbes. However,
decomposer food webs also include higher-level predators that consume fauna of
lower trophic levels, such as those that consume fungi, bacteria, and plant litter. These
predators can induce trophic cascades through changing the density of prey fauna, and
thereby indirectly influence the abundance of bacteria and fungi (Fig. 2.6). Trophic
cascades have long been recognized by soil ecologists to indirectly influence soil
processes driven by soil microorganisms. For instance, Santos et al. (1981) showed
that experimental reduction of predatory tydeid mites enhanced densities of bacterial
feeding nematodes (their main prey source), which in turn reduced rates of microbial
decomposition of plant litter. Several subsequent studies have shown that manipulation

MANIPULATION TROPHIC EFFECTS PROCESS EFFECTS

Santos et al. Reduce tydeid mites Increase bacterial Reduce bacteria Reduce decomposition
(1981) feeding rate
nematodes
Kajak et al. Reduce epigeic Increase litter Increase Increase decomposition
(1993) predators feeding fauna microflora and N mineralisation

Mikola and Add top predatory Reduce microbe No effect on Reduce C and N
Setälä (1998) nematodes feeding microbial biomass mineralisation rate
nematodes
Hedlund and Add predatory mites Likely reduction Enhance hyphal Enhance C
Öhrn (2000) of springtails length mineralisation

Fig. 2.6 Contrasting studies investigating trophic cascades in the decomposer food web, and
the consequences for belowground ecosystem processes.
 2.2 Influence of decomposers • 27

of top predators in the soil food web can affect decomposition and mineralization
of carbon and nitrogen positively (e.g. Allen-Morley and Coleman 1989; Hedlund and
Öhrn 2000), neutrally (e.g. Martikainen and Huhta 1990) or negatively (e.g. Wyman
1998). Moreover, indirect cascading effects of top predators on soil microorganisms
and processes have been shown to occur for a range of types of predators operating at
different spatial scales, including predatory nematodes (Allen-Morley and Coleman
1989), predatory mites (Hedlund and Öhrn 2000; Lenoir et al. 2007), spiders (Kajak
et al. 1993; Lensing and Wise 2006) and salamanders (Wyman 1998). These effects can
occur even when lower trophic levels of the soil food web are unresponsive to
predators, so long as the predators influence the turnover and production of organisms
in the lower trophic levels (Mikola and Setälä 1998a).
The indirect effects of predator-induced trophic cascades on decomposition and
nutrient mineralization in turn have the potential to regulate the availability of
nutrients for plants, and therefore conceivably affect plant nutrient acquisition and
growth. As discussed earlier in this chapter, it is well established that saprotrophic
and microbe-feeding soil fauna have marked effects on plant nutrition and product-
ivity. However, the indirect effect of their predators on plant growth has only been
investigated in two studies by Laakso and Setälä (1999a, 1999b). In both studies,
experimental microcosms containing planted seedlings of Betula pendula were set up
with different soil faunal communities, and these included microcosms with or
without top predatory mites that feed upon microbial-feeding nematodes and sap-
rophagous mesofauna. In both studies, there was no effect of these predators on plant
production, although one of these studies (Laakso and Setälä 1999b) also found no
effect of predators on the basal trophic level of the soil food web (i.e. soil microbes),
indicative of a weak or non-existent trophic cascade in the microcosms. It is possible
that in those situations in which trophic cascades in soil food webs are much stronger
and have more pronounced effects on soil nutrient availability, plant growth might
indeed be responsive to top soil predators.
The variable response of belowground processes to predator-induced trophic
cascades points to these responses being determined by environmental context.
Consistent with this, Lensing and Wise (2006) found that cascading effects of spiders
on plant litter decomposition depended on moisture regime, and were important at a
high-rainfall site with reduced moisture addition, but not at a high-rainfall site with
ambient moisture addition or at a low-rainfall site. Further, Lenoir et al. (2007) showed
that trophic cascades involving top predators, notably gamasid mites, were important
in indirectly influencing soil microflora in soil from a low-fertility site, but not in soil
from a high fertility site. Environmental context can also influence the occurrence and
importance of trophic cascades in soil food webs through influencing the types of soil
organisms present. For example, there is evidence that trophic cascades are more
important in soil food webs dominated by bacteria and bacterial-feeding organisms
than in those dominated by fungi and fungal-feeding organisms (Wardle and Yeates
1993). Further, with the exception of obligate predators such as spiders and centi-
pedes, soil animals with large body sizes are unlikely to induce trophic cascades
because they interact with lower trophic organisms in a mutualistic rather than an
28 • 2 Biotic interactions as ecosystem drivers

antagonistic (i.e. predator–prey) manner. Given that there is much variation across
habitats in the body-size distribution of soil fauna (Wardle 2002), there is also likely to
be much variation in the importance of predator-induced cascades. In any case, much
remains unknown about the types of environmental conditions that are most likely to
favour a dominant role of predator-induced trophic cascades in driving soil processes,
or in which types of ecosystems they should be the most important.

2.2.4 Bacterial-based and fungal-based energy channels and

nutrient cycling
Another approach to the study of soil food webs and their significance for nutrient
cycling and plant production is focused on food web energy channels; these channels
differ in how they influence the availability of nutrients. Moore et al. (1988) proposed
the existence of root, bacterial and fungal energy channels: the root channel consists
of root-associated fauna and symbiotic microbes, while the bacterial and fungal
energy channels consist of organisms that derive their energy from detritus
(Fig. 2.7) (Moore et al. 1998). Moreover, it has been proposed that bacterial and
fungal energy channels have distinct functions, representing ‘fast’ and ‘slow’ cycles
of nutrient availability, respectively (Coleman et al. 1983; Moore and Hunt 1988). As
a consequence, ecosystems dominated by bacterial channels are characterized by
having high nutrient availability and low amounts of nutrient-rich organic matter (e.g.
narrow carbon-to-nitrogen ratio), resulting in part from elevated biological activity,
whereas those dominated by fungal channels often have acid soils of high organic
matter content and low resource availability and quality (e.g. high carbon-to-nitrogen
ratio). This was confirmed by a recent meta-analysis of global data on soil microbial
communities by Fierer et al. (2009), who showed that coniferous forest soils had the
greatest fungal to bacterial ratios, whereas soils from deserts and grasslands had the
lowest. Moreover, across the range of soils examined, the soil fungal to bacterial ratio
was positively correlated with the soil carbon-to-nitrogen ratio (Fig. 2.8), although
this might reflect the integrated effects of a suite of other soil characteristics,
including soil pH, soil organic matter content, and the quality of plant carbon inputs
entering the soil (Bardgett and McAlister 1999; Van der Heijden et al. 2008; Fierer
et al. 2009). Importantly, these types of energy channels are interchangeable: the
fungal channel often becomes increasingly important as primary succession proceeds
(Ohtonen et al. 1999; Neutel et al. 2002; Bardgett et al. 2007a) and following land
abandonment (Zeller et al. 2001; Van der Wal et al. 2006), whereas the bacterial
channel becomes increasingly important following intense disturbance, nutrient
enrichment, heavy grazing by aboveground herbivores, tillage, and intensive farming
(Hendrix et al. 1986; Bardgett and McAlister 1999; Bardgett et al. 2001b; Van der
Wal et al. 2006; R. Smith et al. 2008).
The functional significance of shifts between the fungal- and bacterial-based
energy channel for plant community dynamics is poorly understood. However, it
has been proposed that the bacterial-based energy channel enhances rates of nutrient
mineralization and the availability of nutrients to plants, whereas the fungal-based
 2.2 Influence of decomposers • 29

Decrease NPP
Widen C:N

Labile Decrease N mineralisation Resistant

detritus detritus

Bacteria Fungi Bacteria Fungi

Bacterial Fungal Bacterial Fungal

feeders feeders feeders feeders

Predators Predators
Increase N mineralisation
‘Fast Cycle’ ‘Slow Cycle’
Increase NPP
Narrow C:N

Fig. 2.7 Simplified bacterial and fungal energy channels of the belowground food web. The
bacterial energy channel represents the ‘fast cycle’ due to the higher turnover rates of bacteria
and their consumers relative to the fungi and their consumers, whereas the fungal energy
channel represents the ‘slow cycle’. Changes in the C:N ratio of the detritus, net primary
production (NPP), disturbance, or rates of nitrogen mineralization have been associated with
shifts in the relative dominance of one channel to the other. From Moore et al. (2003), with
permission from the Ecological Society of America.

energy channel promotes ‘slow’ and highly conservative cycling of nutrients

(Coleman et al. 1983; Wardle 2002). This is supported by evidence that decomposer
fungi are highly conservative in their use of nutrients and immobilize substantial
quantities of nutrients in their hyphal networks (Boddy 1999), whereas bacteria have
a more exploitative nutrient use strategy through rapid use of newly produced labile
substrates, for example from plant roots (Bardgett 2005). Further, because bacterial
tissues have low carbon-to-nutrient ratios and concentrations of defence chemicals
relative to fungal tissues, bacterial tissues are consumed by their predators to a much
greater extent, leading to greater nutrient release and turnover (Wardle and Yeates
1993; Wardle 2002).
A growing number of studies show that increases in the abundance of fungi relative
to bacteria within the microbial community are associated with reduced rates of
nutrient mineralization, and vice versa. For instance, Bardgett et al. (2006) showed
that the presence of the hemiparasite Rhinanthus minor in temperate grassland
increased plant diversity and caused a shift in the composition of the microbial
community towards increasing dominance of bacteria relative to fungi, which was
paralleled by a substantial increase in rates of nitrogen mineralization in soil (Fig. 2.9).
30 • 2 Biotic interactions as ecosystem drivers

1
Desert
r 2 = 0.65 Tundra
y = 0.008e0.11x Temperate grassland
Temperate deciduous forest
P = 0.01 Temperate coniferous forest
Fungal: bacterial ratio

0.1

Temp.
Temp. conif.
decid. forest
forest
0.1 Tundra Temp.
grassland
Desert
0.01

0.01

0 10 20 30 40
Soil C : N ratio

Fig. 2.8 Relationships between fungal to bacterial ratios estimated using quantitative poly-
merase chain reaction and soil C:N ratios across five biomes. A fungal:bacterial ratio of
1 means that fungal and bacterial rRNA gene copies are in equal abundance. The bar chart in
the insert shows averages and standard errors of the fungal:bacterial ratios determined for each
of the five biomes. From Fierer et al. (2009), with permission from Wiley-Blackwell.

Consistent with this, Högberg et al. (2007) studied a range of boreal forests of contrasting
nitrogen availability and nitrogen-loading, and found a strong negative correlation
between gross nitrogen mineralization and the fungal-to-bacterial biomass ratio. Further,
Wardle et al. (2004b) studied a series of long-term chronosequences around the globe
(spanning from 6000 to over 4 million years) for which declines in standing plant
biomass had occurred over time, and found that this decline was associated with
increasing substrate phosphorus limitation for microbes and an increase in dominance
of fungi relative to bacteria. In that study, these changes were associated with reduced
rates of litter decomposition and nutrient mineralization, indicative of a negative feed-
back involving further intensified nutrient limitation and ultimately reduced ecosystem
productivity.
Studies are also emerging to support the view that the fungal-based energy channel
is more effective than the bacterial energy channel in promoting nutrient retention,
and this has implications for the nutrient balance of soil. For example, an in situ
15
N-labelling study by Bardgett et al. (2003) showed that the uptake and retention of
added 15N-glycine and ammonium by the microbial community was significantly
greater in unfertilized low-productivity grassland with fungal-dominated microbial
communities than in adjacent fertilized grassland that had a greater relative abundance
 2.2 Influence of decomposers • 31

(a)
1.5

(mg N g–1 dry soil day–1)

1.2

N mineralisation
0.9

0.6

0.3

0
(b)
0.075
Fungal-to-bacterial ratio

0.07

0.065

0.06

0.055

0.05
None 30. 60.
R. minor (plants m–2)

Fig. 2.9 The impact of the hemiparasite Rhinanthus minor on (a) rates of soil nitrogen
mineralization and (b) the fungal-to-bacterial biomass ratio, calculated using phospholipid
fatty acid analysis (PLFA). Values are means and standard errors. From Bardgett et al. (2006),
with permission from Macmillan Publishers Ltd.

of bacteria. Using the same soils, Gordon et al. (2008) found that the fungal-rich
soil was better able to retain nutrients under drying/wetting disturbance than was the
soil with a greater bacterial contribution. Moreover, the increased nutrient loss
from improved soils was associated with a marked decline (45% relative to control)
in microbial biomass nitrogen, suggesting that bacterial-dominated communities
are more sensitive to disturbance than are their fungal-rich counterparts. Other
evidence that shifts in microbial composition relate to changes in nutrient cycling at
the field scale comes from the study by de Vries et al. (2006) of a range of grassland
sites in The Netherlands. These authors found that a higher fungal biomass in soil was
associated with reduced nitrogen leaching and improved nitrogen balance in soil,
suggesting a positive effect of fungi on nutrient retention. While other soil physico-
chemical factors might contribute to the patterns explained above, these studies
collectively point to grassland soils with fungal-dominated microbial communities
being more efficient in retaining nutrients than are their bacterial-dominated
counterparts.
32 • 2 Biotic interactions as ecosystem drivers

It is important to note that bacterial and fungal energy channels operate simultan-
eously, and hence nutrient availability to plants will be controlled by their relative
dominance, rather than by the influence of just one channel. This is recognized within
the nutrient-enrichment model (Moore et al. 2003) described above, which asserts
that plant growth is regulated by the importance of top-down control by predation
affecting nutrient mineralization through the bacterial energy channel relative to that
of bottom-up control influencing nutrient immobilization through the fungal energy
channel. Because the growth of decomposer fungi is regulated more by the availabil-
ity of resources (i.e. bottom-up control) than by predation (i.e. top-down control),
while the reverse is true for bacteria, nutrient availability to plants will be regulated
simultaneously by both top-down and bottom-up control (Wardle 2002).

2.3 Influence of root-associated organisms on plant

communities and ecosystem processes
The above discussion shows how biotic interactions within the decomposer food web
can indirectly influence the structure and productivity of plant communities through
their effects on decomposition processes and nutrient dynamics. Soil organisms also
have substantial direct effects on vegetation dynamics through the actions of root-
associated biota, including symbionts, parasites, pathogens, and root herbivores. In
this section, we consider the ecological role of these direct effects as drivers of plant
community dynamics. First, we consider the influence on vegetation dynamics of
interactions between plant roots and mutualistic symbionts, namely mycorrhizal
fungi and nitrogen-fixers. Second, we examine the role of parasites, pathogens, and
root herbivores as drivers of vegetation dynamics.

2.3.1 Microbial symbionts and plant community dynamics

Perhaps the most well-known belowground symbiotic relationship is that which
occurs between plant roots and nitrogen-fixing bacteria; these bacteria form nodules
in plant roots and convert atmospheric nitrogen into ammonium, thereby making the
nitrogen available to the plants. The most well-known nitrogen-fixing plants are
the legumes which associate with bacteria of the genus Rhizobium, but many non-
leguminous nitrogen-fixing plants also exist, such as those of the genera Casuarina,
Myrica, Hippophae, and Alnus, which associate with actinomycetes of the genus
Frankia. The beneficial effects of nitrogen-fixing bacteria for nitrogen cycling and
plant productivity and nitrogen capture are well documented in both agricultural and
natural settings (Tilman et al. 1997; Cleveland et al. 1999; Spehn et al. 2002; Rochon
et al. 2004; Hopkins and Wilkins 2006; Van der Heijden et al. 2006a). However, their
contribution to plant productivity is believed to be greatest in tropical savannah, and
some grasslands and tropical forests that are dominated by legumes; in these situ-
ations, nitrogen-fixing bacterial symbionts of the legumes can contribute up to 20%
 2.3 Influence of root-associated organisms • 33

of all plant nitrogen that is annually acquired by vegetation (Cleveland et al. 1999;
Van der Heijden et al. 2008).
It was recently proposed by Houlton et al. (2008) that the high abundance of
symbiotic nitrogen-fixing plants in the tropics compared to mature nitrogen-limited
forests of temperate and boreal zones was due to the ability of nitrogen-fixers
to invest nitrogen into phosphorus acquisition, which is a clear advantage in phos-
phorus-limited tropical savannas and lowland tropical forests. In contrast, it was
suggested that modern-day temperatures should constrain nitrogen-fixation rates
and exclude nitrogen-fixing species from mature forests at high latitudes (Houlton
et al. 2008). However, as described below, relatively high rates of nitrogen fixation
performed by cyanobacteria associated with feathermosses may be widespread in
old-growth, high-latitude boreal forests (Zackrisson et al. 2004). It was also recently
suggested by Menge et al. (2008) that the absence of symbiotic nitrogen-fixers in
nitrogen limited temperate and boreal ecosystems could be explained by evolutionary
trade-offs, whereby low nutrient use efficiency, high mortality (or turnover) rate and
low losses of plant-unavailable nitrogen all increase the likelihood that nitrogen
fixation will be selected against (Menge et al. 2008). However, as stressed by these
authors, better characterization of these parameters in multiple ecosystems is neces-
sary to determine whether these mechanisms explain the lack of symbiotic nitrogen-
fixers and thus the maintenance of nitrogen limitation in old-growth forests.
Symbiotic associations between nitrogen-fixing bacteria and plants also play a key
role in vegetation succession, by raising soil nitrogen contents during early succes-
sion to levels needed to support later successional species (Chapin et al. 1994; Kohls
et al. 2003; Walker and del Moral 2003) (Fig. 2.10). For instance, during primary
succession on glacial moraine in Alaska, nitrogen-fixing Alnus shrubs are known to
increase soil nitrogen and organic matter content, thereby creating a more favourable
environment for later successional tree species, especially Picea (Crocker and Major
1955; Chapin et al. 1994). Further, in New Zealand sand dunes, Lupinus herbs have
been shown to facilitate the growth of Pinus trees through a similar mechanism of
nutrient enhancement (Gadgill 1971), while the shrub Hippophäe has been found to
promote plant biomass of later successional species in coastal Dutch sand dunes (Olff
et al. 1993). Further, Bellingham et al. (2001) used field and glasshouse studies to
show that litter from the pioneer nitrogen-fixing legume Carmichaelia odorata, as
well as soil modified by the legume, both significantly promoted growth and nitrogen
uptake by later successional tree species in a New Zealand montane river valley. As
will be discussed further in Chapter 5, the invasion of nitrogen-fixing plant species
into nitrogen-limited ecosystems can also dramatically enhance soil nitrogen avail-
ability and plant productivity, with far-reaching consequences for community and
ecosystem properties (Vitousek and Walker 1989; Sprent and Parsons 2000). The
influence of nitrogen-fixers on vegetation dynamics is also potentially affected by
other organisms, both aboveground and belowground. For instance, the transfer of
nitrogen between legumes and grasses has been shown to occur through hyphal
networks of arbuscular mycorrhizal fungi (Haystead et al. 1988), and it has been
suggested that this route is of nitrogen transfer is of most importance in nitrogen-limited
34 • 2 Biotic interactions as ecosystem drivers

(a) (b) (c)

Fig. 2.10 Dominant N-fixing plants of different primary seres: (a) Alnus sinuata, which forms
thickets on deglaciated terrain at Glacier Bay, south-east Alaska; (b) Coriaria arborea colon-
izing recently deglaciated terrain at the Fox Glacier, South Island, New Zealand; and
(c) Coriaria arborea colonizing floodplains near Kaikoura, South Island, New Zealand.
Images by Richard D. Bardgett.

pioneer plant communities where legumes are often strongly mycorrhizal (Haystead
et al. 1988). The transfer of nitrogen from nitrogen-fixing legumes to neighbouring
grasses has also been shown to be enhanced by infestation of legume roots by host-
specific parasitic nematodes, resulting in increased growth of the neighbouring grass
(Bardgett et al. 1999a; Denton et al. 1999; Dromph et al. 2006; Ayres et al. 2007) with
potential consequences for plant competitive interactions.
Free-living and associative nitrogen-fixing bacteria, which are ubiquitous in terres-
trial ecosystems, can also contribute greatly to ecosystem nitrogen budgets. Although
this input is usually relatively small (<3 kg nitrogen ha1 year1) (Cleveland et al.
1999), it may nevertheless represent the main ecosystem nitrogen input in ecosystems
that experience low nitrogen deposition and lack symbiotic nitrogen-fixers. For
example, nitrogen-fixing cyanobacteria can greatly contribute to the nitrogen econ-
omy of terrestrial ecosystems, such as recently exposed glacial terrain (Schmidt et al.
2008) and boreal forests, where nitrogen fixation has traditionally been thought to be
extremely limited. For example, DeLuca et al. (2002b) showed that nitrogen-fixing
cyanobacteria which inhabit the incurves of leaves of the feather moss Pleurozium
schreberi fix significant quantities of nitrogen (1.5–2.0 kg nitrogen ha1 year1)
and acts as a major contributor to nitrogen accumulation and cycling in boreal forests,
especially in late successional systems and old-growth forests (Zackrisson et al. 2004;
Lagerström et al. 2007; Gundale et al. 2010) (Fig. 2.11). This finding is of high
significance because P. schreberi is the most common moss on Earth, and accounts
 2.3 Influence of root-associated organisms • 35

(a) (b)

Fig. 2.11 Nitrogen-fixing cyanobacteria which inhabit the incurves of leaves of the feather
moss Pleurozium schreberi fix significant quantities of nitrogen and acts as a major contributor
to nitrogen accumulation and cycling in boreal forests, especially in late successional systems
and old-growth forests. (a) Under light microscope; and (b) ultraviolet-fluorescence micro-
graph with a green filter. Coiled chains of Nostoc are hidden in the leaf under light microscopy,
but are readily observed as the red cells under ultraviolet-fluorescence microscopy with a green
filter. Images by P. Lundgren and U. Rasmussen, with permission from Macmillan Publishers Ltd.

for as much as 80% of the ground cover in boreal forests (DeLuca et al. 2002b).
Biological soil crusts, which are assemblages formed by lichens, mosses, liverworts,
cyanobacteria, and other microorganisms, also play key roles in the nitrogen economy
of arid and semi-arid ecosystems worldwide (Belnap 2003; Belnap and Lange 2003;
Bowker et al. 2010). Not only do biological soil crusts fix nitrogen in these ecosys-
tems, but they also influence processes of nitrification and other transformations of
nitrogen (Belnap 2003; Maestre et al. 2005; Bowker et al. 2010).
Another important group of plant symbionts are the mycorrhizal fungi, which are
widespread and associate with roots of some 80% of all terrestrial plant species
(Smith and Read 1997). There are three main groups of mycorrhizal fungi, namely
the arbuscular mycorrhizal fungi, the ectomycorrhizal fungi, and the ericoid mycor-
rhizal fungi. Numerous studies demonstrate their capacity to enhance nutrient supply
to plants, as well as to provide resistance to pathogens, insectivorous herbivores, and
drought (Gange and West 1994; Newsham et al. 1995b; Smith and Read 1997). For
36 • 2 Biotic interactions as ecosystem drivers

instance, studies in grassland show that arbuscular mycorrhizal fungi can enhance
plant productivity by up to two-fold (Van der Heijden et al. 1998b; Vogelsang et al.
2006), a response that is mostly attributed to enhanced plant uptake of phosphorus
plants (Van der Heijden et al. 1998, 2006b), although acquisition of nitrogen through
arbuscular mycorrhizal fungi might also play a role (Hodge et al. 2001; but see
Reynolds et al. 2005; Van der Heijden et al. 2006b). Likewise, ectomycorrhizal fungi
play a crucial role in plant nutrient acquisition in many boreal and temperate forest
ecosystems (Read and Perez-Moreno 2003). Here, organic nutrients contained in
litter and humus are mobilized by extensive ectomycorrhizal hyphal networks that
forage for nutrients and excrete a range of extracellular enzymes that degrade
complex organic compounds (Fig. 2.12) (Leake and Read 1997). While it is difficult
to experimentally determine the contribution of ectomycorrhizal fungi to nutrient
acquisition in situ, several studies suggest that some 80% of all plant nitrogen in

Fig. 2.12 Extensive ectomycorrhizal hyphal networks forage for nutrients and excrete a range
of extracellular enzymes that degrade complex organic compounds. Image by Damian P.
Donnelly and Jonathan R. Leake, University of Sheffield Department of Animal & Plant
Sciences, UK.
 2.3 Influence of root-associated organisms • 37

boreal forests could be taken up through ectomycorrhizal fungi (Simard et al. 2002;
Hobbie and Hobbie 2006).
In general, the role of different types of mycorrhizal fungi changes with vegetation
succession. It has been proposed that in early succession most colonizing plants are
non-mycorrhizal, and that in mid-succession the dominant herbaceous plants often
have a facultative requirement for arbuscular mycorrhizal fungi, whereas in late
succession, trees and shrubs (which typically dominate the vegetation) often have
an obligate need for ectomycorrhizae (Read 1994). However, this pattern is far from
universal, and in particular many late successional forests are also dominated largely
or exclusively by arbuscular mycorrhizal tree species. Importantly, interactions
between mycorrhizal fungi and other symbionts might also act as important regu-
lators of plant production. For instance, legumes commonly form associations with
both arbuscular mycorrhizal fungi and rhizobia (Scheublin et al. 2004), potentially
benefitting from the characteristics of both (Pacovsky et al. 1986). The importance of
such mycorrhizal–rhizobia interactions for plant community dynamics has seldom
been explored.
Mycorrhizal fungi also play a significant role in structuring plant communities, and
in many cases (though not all, e.g. Stampe and Daehler 2003; Van der Heijden et al.
2006b) enhance plant species diversity through reducing plant competition intensity
and promoting more equitable distribution of resources within the plant community.
For instance, Grime et al. (1987) manipulated arbuscular mycorrhizal fungi in
grassland microcosms and found that their presence caused a reduction in dominance
of competitive grass species in favour of several subordinate herb species which
benefited from arbuscular mycorrhizal infection, thereby increasing plant species
diversity. Likewise, Gange et al. (1993) showed that selective fungicides which
suppressed arbuscular mycorrhizal fungi in early successional grassland increased
the abundance of competitively dominant grasses at the expense of subordinate herb
species, thereby reducing plant species richness. Variations in mycorrhizal fungal
diversity have also been shown to affect plant productivity and diversity, especially in
nutrient poor situations. For instance, Van der Heijden et al. (1998b) found that plant
diversity and productivity were positively related to arbuscular mycorrhizal fungal
diversity in experimental grassland, a response that was attributed to more efficient
exploitation and partitioning of soil phosphorus reserves in high arbuscular mycor-
rhizal diversity treatments. In support, Maherali and Klironomos (2007) discovered
that there is much functional complementarity between coexisting arbuscular mycor-
rhizal fungal taxa, which acts to enhance plant production. In contrast, Vogelsang
et al. (2006) manipulated arbuscular mycorrhizal fungal diversity in microcosms and
found that plant biomass in treatments inoculated with six arbuscular mycorrhizal
fungi did not differ from that of the most effective single mycorrhizal fungus,
indicative of little functional complementarity among arbuscular mycorrhizal fungal
species. Further, Jonsson et al. (2001) performed an experiment in which ectomycor-
rhizal fungal diversity was varied from one to eight species, and found that the effects
of fungal diversity on tree seedling growth were context-dependent and influenced by
both host plant species and soil fertility. Consistent with other diversity experiments
38 • 2 Biotic interactions as ecosystem drivers

of soil organisms, studies to date indicate that positive responses of plants to

mycorrhizal fungal infection are likely to driven largely by fungal species identity
rather than by species richness per se.
It should be noted that not all studies show arbuscular mycorrhizal fungi to
promote plant productivity and diversity. For instance, in tallgrass prairie, Hartnett
and Wilson (1999) found that the suppression of arbuscular mycorrhizal fungal
infection through the application of a fungicide enhanced plant species diversity.
This response was attributed to a reduction in the abundance of competitively
dominant and obligately mycotrophic C4 tall grasses, and consequent competitive
release of subordinate facultative mycotrophs. Likewise, it was suggested by Connell
and Lowman (1989) that in tropical rainforests, ectomycorrhizal fungal associations
can encourage dominance of particular tree species at the expense of other (arbuscular
mycorrhizal) tree species which are less able to acquire nutrients and tolerate patho-
gen attack, thereby reducing species coexistence. These studies point to an alternative
mechanism through which mycorrhizal fungi can influence plant communities. Here,
differences in host plant responses to fungal colonization by mycorrhizal fungi can
result in changes in plant diversity if the dominant competitors are either more
strongly or more weakly mycotrophic than are their neighbours. Also, it is important
to note that the costs and benefits of maintaining symbiosis with mycorrhizal fungi
vary greatly among plant species: individual plant responses to infection can range
from positive (mutualism) to neutral (commensalism), and even negative (parasitism).
As a consequence, it is has been proposed that symbiosis might be best defined as a
continuum from parasitism to mutualism (Johnson et al. 1997; Klironomos 2003),
and that inter-species differences in the direction and intensity of response to mycor-
rhizal infection along this continuum might act as important (though little explored)
structuring forces in plant communities (Klironomos 2003).

2.3.2 Belowground pathogens, herbivores, and plant

community dynamics
A growing body of literature points to the power of soil pathogens to act as drivers of
spatial and temporal patterns in vegetation (Van der Putten 2003, 2009). The mechan-
ism involved is negative feedback, which operates through the accumulation of specific
plant pathogens that inhibit the growth of the host plant more than that of neighbouring,
non-infected plant species, thereby causing vegetation change (Bever et al. 1997;
Packer and Clay 2000; Van der Putten 2003). It has also been suggested that soil
pathogens can contribute to the maintenance of plant diversity through negative
feedback when it suppresses the growth of dominant plants (Bever et al. 1997).
Conversely, a study by Klironomos (2002) showed that rare plant species were
affected more than dominant plants by negative plant–soil feedback, thereby suggest-
ing that soil pathogens contribute to plant rarity and reduce plant diversity. Several
experimental studies have demonstrated the powerful role of pathogens as drivers of
vegetation dynamics (e.g. Van der Putten et al. 1993; Packer and Clay 2000), and these
are discussed in Chapter 3 in the context of how plant communities affect pathogens
 2.3 Influence of root-associated organisms • 39

and vice versa. With regards to vegetation succession, it has been proposed that effects
of soil pathogens via negative feedback are most prominent during late succession
when plant host densities are greatest, thereby enabling the build up of pathogens in
soil (Reynolds et al. 2003; but see Kardol et al. 2006), as discussed in depth in
Chapter 3. Plant pathogens have also been shown to play an important role in plant
invasion (Wolfe and Klironomos 2005; Reinhart and Callaway 2006; Van der Putten
et al. 2007), as will be described further in Chapter 5.
The soil also contains a wide variety of root-feeding animals, including parasitic
nematodes and insects, which selectively feed on roots mostly on the basis of their
palatability. As with other root-associated organisms, such selective feeding differen-
tially influences the performance of plant species in mixed communities, thereby
altering vegetation dynamics. A classic example of the capacity of belowground insect
herbivores to influence vegetation dynamics is the work of Brown and Gange (1989;
1992), which used selective insecticides to exclude both aboveground and below-
ground insects from grasslands differing in successional stage in southern England.
Their results showed that while aboveground insect herbivory slowed down secondary
succession by preventing perennial grass development, root herbivory enhanced it by
reducing early succession annual forbs. In a similar field experiment in Germany,
Schädler et al. (2004) found that while aboveground insects had no effect on plant
species replacement, belowground herbivory reduced the competitive ability of
resident species, thereby facilitating colonization by late successional species and
secondary succession. In a grassland mesocosm experiment in The Netherlands, De
Deyn et al. (2003) found that belowground nematodes, wireworms, and microar-
thropods enhanced the replacement of early by later secondary succession plant
species and promoted plant diversity, which was attributed to the suppression of
dominant plant species by root-feeding fauna which allowed subordinate plant species
to proliferate.
The influence of root-feeding animals on vegetation dynamics also has the poten-
tial to be manifested through their influence on aboveground herbivores and vice
versa. The topic of aboveground multitrophic interactions as drivers of vegetation
dynamics and ecosystem processes is discussed in Chapter 4, but it should be noted
here that empirical studies have shown root herbivory to strongly influence the
performance of foliage-feeding insects (Gange and Brown 1989; Masters and
Brown 1992; Masters et al. 2001; Bezemer et al. 2004; but see Salt et al. 1996).
Similarly, the performance of root herbivores has been shown to be affected by foliar
herbivores (Masters and Brown 1992; Salt et al. 1996; but see Masters et al. 1993).
Moreover, there is potential for both aboveground and belowground herbivores to
influence vegetation dynamics indirectly through their influence on free-living soil
organisms that regulate nutrient availability to plants. For instance, microcosm
studies show that root-feeding nematodes and foliar herbivory can enhance root
exudation, which in turn stimulates rhizosphere microbial growth and activity, and
alters microbial community composition (Denton et al. 1999; Guitian and Bardgett
2000; Ayres et al. 2007), with likely consequences for nutrient availability. However,
De Deyn et al. (2007) found no effects of aboveground and belowground herbivory
40 • 2 Biotic interactions as ecosystem drivers

by wireworms on decomposer nematodes, although the wireworms did facilitate

root-feeding nematode, which was thought to be driven by shifts in plant species
composition. Most studies to date on this topic have been done under specific and
often artificial conditions, and so the consequences of these complex aboveground–
belowground interactions for vegetation dynamics in real ecosystems are little
understood.

2.4 Soil ecosystem engineers and plant

community dynamics
Soil fauna also affect nutrient cycling and the plant community through physical
alteration of decomposing material and of the soil habitat (Bardgett 2005). Two
groups of soil organisms play a key role. First, the litter transformers consume
plant detritus and egest this material into soil as fecal pellets with a higher surface-to-
volume ratio; this provides a more favourable environment for microbial growth than
does the original leaf litter, and therefore stimulates rates of decomposition and
nutrient release (Webb 1977; Hassall et al. 1987; Zimmer and Topp 2002). Second,
the ecosystem engineers build physical structures in soil that provide habitats for
microbes and other organisms, and also alter the movement of materials through soils
and across ecosystems (Lavelle et al. 1995, 1997; Bardgett et al. 2001a). The role of
litter transformers will be discussed later in this chapter in the context of carbon
dynamics. Here, we focus on how the activities of soil ecosystem engineers, which
include mostly macrofauna, influence vegetation dynamics in terrestrial ecosystems
(Fig. 2.13). We also briefly discuss the role of ecosystem engineers in modifying soil
physical properties, and in affecting the transfer of water and nutrients within soil and
to ground-waters.
The most widely known ecosystem engineers in soil are the earthworms and there is
a huge literature documenting their importance for soil fertility and plant growth in both
natural and agricultural systems (e.g. Lee 1985; Edwards and Bohlen 1996; Scheu
2003; Edwards 2004). These effects arise largely from their role in consuming vast
quantities of plant litter and through their production of surface and subsurface casts,
which provide a more favourable environment for microbial activity and hence nutrient
availability. Benefits also arise through their burrowing activities which integrate plant
litter into the soil and improve its physical structure. The activity of earthworms in soil
can also influence the abundance and distribution of other soil fauna, such as microbe-
feeders and litter transformers (Yeates 1981; Alphei et al. 1996; Binet et al. 1998;
Ilieva-Makulec and Makulec 2002; Tao et al. 2009), with indirect consequences for soil
microbial communities, nutrient availability, and plant growth.
While numerous studies have explored the benefits of such activities for the growth
of single plant species (see Scheu 2003), only a handful have considered the conse-
quences for vegetation dynamics; most of these have been done in grassland systems
and show that, in general, the presence of earthworms favours the growth of fast-
growing grasses over forbs and legumes. For instance, Hopp and Slater (1948) found
 2.4 Ecosystem engineers and plant communities • 41

(a) (b)

(c) (d)

Fig. 2.13 Soil ecosystem engineers and the structures that they produce: (a) mounds of the
soil-feeding termite Cubitermes severus in moist savanna, Nigeria (image by Reine Leuthold);
(b) ant nest in boreal forest, Sweden (image by Richard Bardgett); (c) dung beetles (image by
Rosa Menendez); and (d) casts produced by the earthworm Aporrectodea longa (image by
Kevin Butt).

that earthworms increased the dominance of grasses relative to legumes in experi-

mental grassland systems. Similarly, Hoogerkamp et al. (1983) showed that the
introduction of earthworms into polder soils in which they were previously absent
increased the performance of grasses relative to forbs. Further, Scheu (2003) presented
data showing that perennial ryegrass (Lolium perenne) benefited more from the
presence of earthworms than did white clover (Trifolium repens) in pot experiments.
The mechanism for such effects is not fully understood, but it has been suggested
(Scheu 2003; Wurst et al. 2005), and recently shown (Eisenhauer and Scheu 2008),
that earthworms enhance the competitive ability of grasses against legumes by
increasing the supply of nitrogen for grasses. The promotion of graminoids relative
to other plant functional groups might also result from grasses being more associated
with earthworm casts, where enhanced nutrient availability stimulates their growth
(Zaller and Arnone 1999). Further, grasses may benefit from earthworms causing a
more patchy distribution of soil organic matter; grasses tend to be better able to forage
42 • 2 Biotic interactions as ecosystem drivers

resource patches through root proliferation than are forbs and legumes (Scheu 2003;
Wurst et al. 2003). Earthworms might also influence plant community dynamics by
affecting seed transport and germination, for instance through preferential ingestion of
seeds of certain plant species and sizes, and deposition of them in nutrient-rich casts
(Piearce et al. 1994; Thompson et al. 1994; Scheu 2003). However, very little is
known about the significance of these processes in natural plant communities.
The dominant ecosystem engineers of tropical soils are termites, which can reach
densities as high as 7000 m2 and constitute some 95% of belowground insect
biomass (Aber et al. 2000). Termites feed mainly on decaying organic matter and
roots, and are best known for their large effects on soil nutrient cycling and the
physical architecture and hydrology of soils, through their mound-building and
gallery-excavating activities (Aber et al. 2000; Hyodo et al. 2000). Most termites
depend on symbiotic gut bacteria for energy metabolism, whereas others such as the
‘fungus growers’ (which will be discussed below in the context of carbon cycling)
lack these gut flora and rely on externally cultivated fungi for their nutrition (Aber
et al. 2000). Some termites also contain populations of flagellate protozoa in their
guts that have the ability to degrade cellulose and other plant polysaccharides,
whereas others have gut bacteria which fix atmospheric nitrogen and can potentially
act as an ecosystem nitrogen input (Breznak and Brune 1994; Aber et al. 2000).
Further, termite mounds serve as foci for nutrient redistribution in many landscapes
(Spain and McIvor 1988; Aber et al. 2000). The effects of termites on vegetation
dynamics are most noticeable in ‘termite savanna’ ecosystems, which is a term coined
for vegetation formations in Africa and South America, consisting of grasslands and
discrete islands of woodland based on large termite mounds (Harris 1964). In these
ecosystems, termites can greatly influence vegetation succession. When mounds
become physically stable, either through colony death or because the mound is so
large that only part of it is colonized by termites, a vegetation succession occurs
whereby grasses colonize, and are then replaced by shrubs and finally tall trees. When
favourable conditions permit, these islands of woodland increase in size until they
merge with each other and produce a closed canopy forest (Harris 1964).
Ants similarly influence vegetation patchiness and dynamics by altering soil
physical properties and through the formation of nests. The vast majority of ants
build nests within soil, where they concentrate organic material and create hotspots or
‘oases’ of high nutrient availability which serve to stimulate plant growth and create
vegetation mosaics (Hölldobler and Wilson 1990). For instance, leaf-cutter ants,
which are a principal herbivore of neotropical regions, build large nests which extend
deep into the soil (Hölldobler and Wilson 1990). These nests create patches of high
nutrient availability which promote plant growth, thereby forming vegetation patches
that are distinct from non-nest areas and areas where nests have been abandoned
(Garrettson et al. 1998; Verchot et al. 2003; Moutinho et al. 2003). These types of
positive effect of ant nests on vegetation have been shown to be reversible by natural
fire, particularly in neotropical regions (Sousa-Souto et al. 2008). However, burning in
the neotropics can also facilitate establishment of leaf-cutter ants because they prefer
open terrain (Vasconcelos and Cherret 1995). This greater activity of leaf-cutter ants
 2.4 Ecosystem engineers and plant communities • 43

can in turn encourage greater plant nutrient availability on nutrient depleted soils,
thereby accelerating vegetation recovery after fire (Sousa-Souto et al. 2007). Another
recently discovered mechanism by which leaf-cutter ants influence nutrient cycling in
neotropical ecosystems is via their engagement in mutualistic associations with
nitrogen-fixing bacteria, which supplement the nitrogen budget of the their fungal
gardens that they cultivate for food. Using acetylene reduction and stable isotope
experiments, Pinto-Tomás et al. (2009) showed that nitrogen fixation occurred in the
fungus gardens of a wide range of leaf-cutter ant species, and that this fixed nitrogen
was incorporated into ant biomass (Fig. 2.14). Moreover, they found that symbiotic
nitrogen-fixing bacteria were consistently isolated in fungus gardens of leaf-cutter ant
colonies collected from across several sites in Argentina, Costa Rica, and Panama.
Through this mechanism, the authors estimated that a single mature leaf-cutter ant
colony could contribute as much as 1.8 kg of fixed nitrogen per year into neotropical
ecosystems. Given the dominance of leaf-cutter ants, this could represent major source
of nitrogen in neotropical ecosystems (Pinto-Tomás et al. 2009).
While most ants build nests in soil, a small group of ants, mostly of the genus
Formica, build large parts of their nests on the soil surface using organic materials
such as needles, twigs, and bark collected from the surrounding area (Jurgensen et al.
2008). These surface mound-building ants are common in many temperate and boreal
grasslands and forests in Europe and North America (Hölldobler and Wilson 1990)
where they can have substantial effects on vegetation development and ecosystem
processes. These effects can be direct, for instance through enrichment of organic
matter and nutrients in mounds relative to adjacent soil (Jurgensen et al. 2008). They
can also be indirect, through predation on decomposer fauna or other predators such

(a) (b)
12 c 1.4 b
11
1.2
Acetylene reduction activity

10
(nmol/ethylene/hour/g dw)

d
9
1.0
8
% N content

7 0.8
6
5 e e 0.6
b
4
a 0.4
3
2 0.2
a a a
1
0 0
Fungus Ant Ant Whole Refuse Leaves Fungus Ant Ant
Leaves
Garden Workers Brood Colony Dump Garden Workers Brood

Fig. 2.14 Evidence for nitrogen fixation in the fungus gardens of leaf cutter ants: (a) nitrogen
content of the different components of five leaf cutting ant colonies and (b) nitrogen-fixation
activity measured by acetylene reduction for different components of 10 leaf-cutting ant
colonies. All results are shown as means + SEM. Means labelled with different letters (a–e)
are statistically different (P < 0.05). From Pinto Tomás et al. (2009), with permission from the
American Association for the Advancement of Science.
44 • 2 Biotic interactions as ecosystem drivers

as spiders (Laakso and Setälä 1997; 1998; Hawes et al. 2002), thereby potentially
triggering trophic cascades that influence decomposition processes and nutrient
availability. Mound-building ants can also indirectly influence soil nutrient supply
to plants either by tending and protecting aphids which feed on phloem sugars from
leaves and twigs in tree canopies (Stadler and Dixon 2005; Styrsky and Eubanks
2007), or by attacking leaf-defoliating insects (Warrington and Whittaker 1985).
Both of these activities have the potential to alter the quantity and quality of carbon
inputs to soil from litter and leachates of needles and leaves (Stadler et al. 2001),
and thereby influence soil organisms and the processes of nutrient cycling that they
drive. Further, because ant mounds facilitate colonization and growth by some plant
species above others, they can exert important effects on vegetation composition and
succession. For example, Blanka et al. (2009) showed that mounds formed by the ant
Lasius flavus in Slovakian mountain grasslands supported colonization of spruce
(Picea abies) forest, accelerating succession of grassland to spruce forest. The role of
such aboveground trophic interactions as drivers of soil and vegetation dynamics will
be considered in more detail in Chapter 4.
Ecosystem processes and vegetation dynamics can also be affected by dung
beetles, a widely distributed group of insects which are most abundant in tropical
forests and savannas (Hanski and Cambefort 1991). As will be discussed in Chapter 4,
significant quantities of nutrients are recycled in terrestrial ecosystems via vertebrate
faeces, and the principal role of dung beetles is to transfer into and relocate this
material within the soil, thereby instigating a series of changes that affect soil nutrient
cycling and plant growth (Nichols et al. 2008). For instance, several studies show that
dung beetles stimulate soil microbial activity and rates of nitrogen mineralization
(Yokoyama and Kai 1993; Yokoyama et al. 1991; Yamada et al. 2007), and increase
soil pH, cation exchange capacity, and concentrations of nutrients (e.g. phosphorus,
nitrogen, potassium, calcium, and magnesium) (Yamada et al. 2007). As a conse-
quence, numerous studies have reported beneficial effects of dung beetle activity on
the growth and nutrient content of agricultural crops, and on net primary production
(NPP) in natural settings (Nichols et al. 2008). Moreover, by incorporating dung into
the soil, dung beetles can also help to reduce ecosystem nitrogen loss through
ammonium volatilization, although they can stimulate nitrogen loss by denitrification
through promoting nitrate availability in the soil (Yokoyama et al. 1991). As with
earthworms, dung beetles also have the potential to influence vegetation dynamics
through the relocation of plant seeds, both horizontally and vertically (Nichols et al.
2008). This can benefit seed survival by reducing predation and pathogen attack
and by directing seed dispersal to more favourable microclimates for germination
and emergence (Andresen and Levey 2004). Dung beetles also influence plant
communities indirectly through predation of leaf-cutting ants (e.g. Vasconcelos
et al. 2006), which as discussed above strongly impact on ecosystem processes and
vegetation dynamics in neotropical regions. Before leaving the topic of dung beetles,
it is important to note that most studies on their influence on soil processes and
vegetation have been done in grasslands and agricultural settings, often under
artificial conditions and with single plant and dung beetle species. Their role in
 2.5 Biotic interaction and carbon dynamics • 45

regulating ecosystem processes and vegetation dynamics in natural ecosystems is

hence poorly understood and represents a significant gap in understanding (Nichols
et al. 2008).
Soil macrofauna can substantially modify the physical structure of soil, and in
many cases significantly improve soil porosity and the movement or water and
nutrients through the soil (Bardgett et al. 2001a). For instance, it is well documented
that earthworms increase the density of macropores and channels in soil (Knight et al.
1992; Lavelle et al. 1997), thereby enhancing water infiltration and the movement of
both water and soluble nutrients through soil and to inter-connected waterways
(Sharply et al. 1979; Bardgett et al. 2001a). Similarly, nests of soil-dwelling ants
provide extensive macroporosity to soil, which affects the rates of infiltration of both
water and soluble nutrients (Eldridge 1993). While such improvement in soil porosity
and water movement caused by earthworm burrowing can significantly enhance plant
growth, increased rates of infiltration (especially when caused by deep-burrowing
species) can also cause increased leaching, and hence loss of nutrients from soil. For
example, the inoculation of grain-crop soils with earthworms was found to result in a
4–12-fold increase in leachate volumes and a 10-fold increase in the amount of
dissolved nitrogen contained within them (Subler et al. 1997). Further, the inocula-
tion of limed coniferous forest soils with earthworms was found to cause a 50-fold
increase in the concentration of nitrate and cations in soil solution, therefore greatly
enhancing the potential for nutrient loss for these soils (Robinson et al. 1992; 1996).
Although not quantified, these types of effects of soil animals on water infiltration and
leaching are likely to have strong influences on nutrient availability to plants, and also
on the transfer of water and nutrients to ground-waters and adjacent ecosystems, with
potential consequences for water quality (Bardgett et al. 2001a).

2.5 Soil biotic interactions, carbon dynamics, and

global change
So far, we have considered the role of soil biotic interactions as regulators of nutrient
cycling and plant community dynamics at local scales. However, soil biotic inter-
actions also play a key role in regulating carbon dynamics in terrestrial ecosystems,
with potential global consequences for land–atmosphere exchanges of carbon, and
carbon-cycle feedbacks that could amplify climate change. Soils play a major role in
climate feedbacks because they release and absorb greenhouse gases, such as carbon
dioxide and methane, while storing large quantities of carbon and acting as a
significant global carbon sink (Schimel et al. 1994; Heimann and Reichstein 2008;
Chapin et al. 2009) (Fig. 2.15). Indeed, it has been estimated that soils contain some
80% of the Earth’s terrestrial carbon stock and as much as 90% of the carbon pool of
grasslands, deserts, tundra, wetlands, and croplands (IPCC 2007). The flux of below-
ground carbon dioxide to the atmosphere due to respiration is an order of magnitude
larger than emissions of carbon dioxide through anthropogenic sources (Raich and
Potter 1995; IPCC 2007). Further, there is considerable concern that global warming
46 • 2 Biotic interactions as ecosystem drivers

Fig. 2.15 Soil organic carbon map showing the distribution of the soil organic carbon to
1 m depth. From FAO-UNESCO, Soil Map of the World, digitized by ESRI. Soil climate
map, USDA-NRCS, Soil Survey Division, World Soil Resources, Washington DC.

will increase this liberation of carbon dioxide from soil to atmosphere due to enhanced
microbial breakdown of soil organic matter (Jenkinson et al. 1991; Davidson
and Janssens 2006). Such acceleration in carbon loss could significantly exacer-
bate the soil carbon-cycle feedback if predicted climate change scenarios are correct
(Cox et al. 2000; Friedlingstein et al. 2006). In this section, we discuss the role of soil
biotic interactions in regulating soil carbon flux to the atmosphere, and consider how
such activities contribute to climate change via carbon-cycle feedbacks.

2.5.1 Soil biotic interactions and ecosystem carbon exchange

The vast majority of plant production (80–90%) enters the soil food web as exudates,
dead leaves, roots, wood, or animal wastes. Although abiotic factors, especially
moisture and temperature, act as primary determinants of the rate of decomposition
of this organic matter, soil microbes are directly responsible for its breakdown
because they are often the only organisms in soil that produce enzymes capable of
degrading recalcitrant plant-derived compounds such as lignin and cellulose. As
a consequence, a large proportion (50%) of soil respiration can be attributed to
the activity of heterotrophic microbes, the remainder being due to plant roots
(autotrophic respiration) and associated mycorrhizal fungi (Högberg and Read
2006). While a large amount of respiration can be attributed directly to heterotrophic
microbes, there is ample evidence that biotic interactions between microbes and
animals, including collembolans, mites, enchytraeids, isopods, and earthworms,
 2.5 Biotic interaction and carbon dynamics • 47

indirectly stimulate rates of organic matter decomposition and respiration through a

variety of mechanisms (Mikola et al. 2002; Wardle 2002; Bardgett 2005; Cole et al.
2006). First, they fragment plant material, which increases the surface area available
for microbial colonization (Swift et al. 1979; Seastedt 1984; Wardle 2002; Bardgett
2005). Second, they partially digest dead plant matter and return the rest of it to the
soil as faecal pellets which have a higher surface-to-volume ratio and provide a more
favourable environment for microbes than does the original material consumed; this
in turn enhances rates of decomposition and nutrient release (Webb 1977; Teuben
and Verhoef 1992; Zimmer and Topp 2002; Zaady et al. 2003). Third, they bring
decomposer microbes and organic matter into more direct contact. For example, the
guts of termites and earthworms provide a microenvironment in which microbes form
symbiotic relationships with their host through producing extracellular enzymes that
break down recalcitrant organic compounds, thereby making nutrients more access-
ible to the host (Zimmer and Topp 1998; Slaytor 2000; Dillon and Dillon 2004).
Some fauna, such ants, also concentrate carbon in their nests, which consequently
have higher rates of respiration than adjacent areas (Risch et al. 2005; Ohashi et al.
2007), although it is not known how much this contributes to total soil carbon dioxide
emissions (Jurgensen et al. 2008).
The positive effect of soil macrofauna on decomposition through bringing mi-
crobes and organic matter into closer contact does not end in the gut. Microbes from
the gut are also released in faecal material where they continue to decompose egested
organic matter (Frouz et al. 2002; 2003). Further, some fauna such as termites and
leaf-cutting ants play an important role in bringing plant matter into contact with
decomposers through their external symbioses with fungal saprotrophs. For example,
termite populations and fungal combs (i.e. ‘gardens’) have been found to account for
between 5 and 39% of the annual respired litter carbon in tropical savannah and dry
tropical forest (Yamada et al. 2005). Similarly, earthworms are known to drag litter
from the soil surface into burrows, thereby increasing its availability to soil microbes
and enhancing its decomposition (Tiunov and Scheu 1999). As discussed above,
dung beetles also play a crucial role in enhancing rates of decomposition and nutrient
availability both by stimulating microbial activity and by relocating mammal faeces
and carrion into soil (Yokoyama et al. 1991; Nichols et al. 2008). This may be
especially important in tropical forests where they are capable of transferring all
deposited faeces into soil within hours of deposition (Arrow 1931; Slade et al. 2007),
resulting in enhanced rates of organic matter decomposition and soil respiration
(Stevenson and Dindal 1987). Likewise, earthworms consume vast amounts of both
plant litter and soil mineral particles, which are mixed together in the earthworm gut
and egested as surface and subsurface casts. Such casts, which can be produced at
annual rates ranging from 1 to 500 t ha1, contain greater numbers of microbes and
have higher enzyme activities than does surrounding soil (Edwards and Bohlen
1996). As a consequence, the presence of earthworms is well known to enhance
rates of decomposition and carbon mineralization (Cortez et al. 1989), and rates of
nitrogen and phosphorus mineralization (Scheu 1987; Lavelle and Martin 1992;
Sharpley and Syers 1976).
48 • 2 Biotic interactions as ecosystem drivers

Another mechanism by which animals influence soil respiration and carbon diox-
ide release is through their feeding activities. As discussed previously, the primary
food source of many soil animals are microorganisms. Faunal grazing on microbes
can markedly affect the growth, activity, and composition of microbial communities
with important consequences for decomposition and soil respiration. For instance,
low and intermediate levels of grazing by collembolans have been shown to stimulate
the growth, respiration, and enzyme production of decomposer fungi (Hanlon and
Anderson 1979; Bengtsson and Rundgren 1983; Hedlund et al. 1991; Bardgett et al.
1993c), in some cases leading to enhanced litter mass loss (Cragg and Bardgett 2001).
Also, grazing by nematodes, protozoa, and mites has been shown to influence the
activity and growth of soil bacteria and fungi (Dyer et al. 1992; Vreeken-Buijs et al.
1997; Hedlund and Öhrn 2000; Bonkowski 2004), which is in turn likely to alter rates
of organic matter decomposition. Further, selective feeding by collembolans has been
shown to alter fungal community structure, with consequences for ecosystem level
processes such as plant litter decomposition (Newell 1984a, 1984b). Collectively,
these studies point to biotic interactions between microbial-feeding fauna and mi-
crobes as important drivers of organic matter decomposition and carbon exchange in
terrestrial ecosystems.
Most of the aforementioned studies have considered the influence of single species
or functional groups of soil organisms on aspects of the carbon cycle. As discussed
above, there is potential for trophic cascades within the soil food web to influence
organic matter decomposition. However, studies that have explored how variations in
the diversity and composition of the soil community influence decomposition pro-
cesses and respiration mostly point to the important role of species traits as drivers of
these processes. For instance, Cragg and Bardgett (2001) used three species of
collembolans to create model communities of one, two, or three species in all possible
combinations, and found that rates of soil respiration were better explained by the
presence versus absence of one species (Folsomia candida) than by species richness
per se. Likewise, Heemsbergen et al. (2004) found that species richness of experi-
mental soil macrofauna communities (ranging from one to eight species) was a poor
predictor of the rates of litter mass loss and soil respiration. However, they also found
that the functional dissimilarity of species explained much of the variation in these
processes (Fig. 2.16). The positive effect of functional dissimilarity on decomposition
processes that they observed was attributed to facilitative interactions between com-
ponent species, which were greatest when component species had different functional
roles (Heemsbergen et al. 2004). These findings suggest that to predict the conse-
quences of species loss on decomposition processes first requires an understanding
of how individual species contribute to multiple species interactions. In cases where
diversity effects on decomposition processes have been found, they tend to occur at
the lower end of the diversity gradient (Liiri et al. 2002; Setälä and McLean 2004;
Tiunov and Scheu 2005), pointing to a high degree of functional redundancy within
soil communities (Liiri et al. 2002; Setälä and McLean 2004). However, as discussed
earlier in the chapter some species are more redundant than others, and some are
functionally irreplaceable (Laakso and Setälä 1999a,b).
 2.5 Biotic interaction and carbon dynamics • 49

(a)

40

20

10

–10
Net diversity effect

–20
4 6 8 10 12 14 16 18
(b)

60

40

20

–20

0 2 4 6 8 10 12 14 16
Mean functional dissimilarity

Fig. 2.16 Influence of macro-detritivore diversity in experimental communities on soil res-

piration (a) and leaf-litter mass loss (b) in relation to mean functional dissimilarity, defined as
the degree to which component species are functionally different in those processes determined
from their performance in monoculture. Each series of dots represents a treatment (n ¼ 5
replicates per treatment; some dots overlap). A significant positive regression between the
mean functional dissimilarity of the communities and the net diversity effect for soil respiration
and leaf-litter mass loss indicates that positive net diversity effects are more pronounced in
communities consisting of functionally dissimilar species. Functional dissimilarity was related
to neither species number nor taxonomic group number. From Heemsbergen et al. (2004), with
permission from the American Association for the Advancement of Science.
50 • 2 Biotic interactions as ecosystem drivers

It is important to recognize that the role of soil biotic interactions relative to abiotic
factors that regulate decomposition processes and carbon exchanges varies tremen-
dously across biomes. For instance, in a comparative study across ecosystems,
Gonzalez and Seastedt (2001) found that the role of soil fauna in governing decom-
position was disproportionally greater in tropical wet forests than in tropical dry or
subalpine forests. Likewise, Wall et al. (2008) conducted a global decomposition
experiment to assess the importance of soil animals in carbon mineralization across
30 sites distributed from 438S to 688N on six continents, and found that soil animals
increase decomposition rates in temperate and wet tropical climates, but have neutral
effects where temperature or moisture constrains biological activity. Overall, these
findings were taken to suggest that faunal influences on decomposition processes are
dependent on prevailing climatic conditions, and are therefore of most relevance at
the regional scale when attempts are made to predict the effects of global change
scenarios on carbon dynamics (Wall et al. 2008) (Fig. 2.17). In contrast, Powers et al.
(2009) found for 23 tropical forest sites that variation in annual rainfall among sites
from 760 to 5797 mm per year had no effect on whether mesofaunal exclusion altered
decomposition, even though precipitation was strongly related to decomposition rate.
The relationship between macroclimate and faunal effects on decomposition is
complicated further by the fact that the complexity of soil communities also varies
greatly across biomes, and it has been suggested that decomposition processes may
be especially susceptible to changes in soil diversity in species poor soils of extreme
environments such as hot and cold deserts (Freckman and Mankau 1986; Freckman
and Virginia 1997; Wall 2007).
While soil respiration is typically separated into autotrophic and heterotrophic
components, it is in reality driven by a continuum from roots with their autotroph-
dependent mycorrhizal fungi, through to other rhizosphere microorganisms that are
supported largely by recent photosynthates, to the classical heterotrophs discussed
above that decompose larger macromolecules in soil organic matter (Fig. 2.18)
(Högberg and Read 2006). There is now mounting evidence that the autotroph-linked
component of this continuum, which is fueled by recent photosynthate, is as import-
ant a driver of carbon exchange as are the much slower fluxes of carbon arising from
the decomposition of plant litter (Högberg and Read 2006). There are two broad
lines of evidence that support this view. First, as discussed further in Chapter 3,
field experiments using physiological manipulations (e.g. tree-girdling) and canopy-
labelling techniques show that as much as half of the soil respiratory carbon release
from soil is derived from recent photosynthate fixed over the previous hours or days
(Craine et al. 1999; Högberg et al. 2001; Steinmann et al. 2004; Pollierer et al. 2007).
Second, mycorrhizal fungi which colonize around 80% of land plants and support
vast extraradical mycelial systems provide the largest sink for these photosynthates
(Johnson et al. 2002; Leake et al. 2004). The onward transfer of this recent photo-
synthate from hyphae to the soil occurs by respiration and exudation from hyphal tips
as labile organic compounds such as sugars, low-molecular-weight carboxylic acids,
and amino acids (Johnson et al. 2002; Jones et al. 2004), and by grazing of hyphae by
fungal-feeding animals. For instance, Johnson et al. (2005) showed that the addition of
 2.5 Biotic interaction and carbon dynamics • 51

Neutral Faunal Effect N

W E
Fauna Enhanced Decomposition S

Fig. 2.17 Map showing climatic regions where soil animals were found to enhance decom-
position rates, adapted from Wall et al. (2008). Results from temperate and wet tropical
climatic regions (light gray) show fauna to increase decomposition rates, but to have neutral
effects in other regions (dark gray). This suggests that in future scenarios of climate change for
regions predicted to be warmer and wetter, enhanced decomposition rates may result from
greater effects of soil animals and other biota. Results are based on the Global Litter
Invertebrate Decomposition Experiment (GLIDE). From Wall et al. (2008), with permission
from Wiley-Blackwell.

Recent More complex,

photosynthate C macromolecular C

Saprotrophic
ECM fungus
fungus

ECM roots and their Bacteria (B) in the True heterotrophic

extraradical mycelia plus vicinity of ECM microorganisms and
somebacteria in the hyphae soil organisms at
mycorrhizosphere higher trophic levels

Fig. 2.18 The soil autotroph–heterotroph respiratory continuum. Movement to the right
means a decreasing use of recent photosynthate, but increasing heterotrophy and metabolism
of carbon of increasing ‘age’ (i.e. time since incorporation of carbon during photosynthesis).
ECM, ectomycorrhizal. From Högberg and Read (2006), with permission from Elsevier.
52 • 2 Biotic interactions as ecosystem drivers

fungal-feeding collembolans to grassland soils disrupted arbuscular mycorrhizal

fungal networks in grassland and reduced 13C-enrichment of mycorrhizosphere res-
piration by 32%, indicating that the presence of some soil fauna may inhibit carbon
fluxes through certain pathways. In addition, grazing of mycorrhizae by soil fauna can
result in positive (Setälä 1995) or negative (Finlay 1985) effects on plant growth,
which could in turn influence the supply of recent photosynthate to the mycorrhizal
fungi and soil. As noted by Högberg and Read (2006), these processes occur within the
same microscale as the decomposition of detritus by heterotrophic microorganisms,
creating difficulties in discriminating between the activity of autotroph-dependent
mycorrhiza and that of heterotrophs. However, these new insights emphasize the role
of plant canopy processes, living roots, their symbiotic fungal partners and other
closely associated microbes, and soil fauna, as determinants of soil activity and
respiratory release of carbon (Högberg and Read 2006; Pollierer et al. 2007).

2.5.2 Contribution of soil biotic interactions to climate change

via carbon-cycle feedbacks
Ultimately, the net effect of climate change on ecosystem carbon budgets depends on
the balance between photosynthesis and both autotrophic and heterotrophic respir-
ation. Although our knowledge of the assimilatory component (i.e. photosynthesis) of
the carbon cycle and its response to climate change is well advanced, there are major
gaps in our understanding of the response of soil respiration (Trumbore 2006).
Climate change has both direct and indirect effects on the activities of soil organisms
that return greenhouse gases to the atmosphere and contribute to global warming.
Direct effects include the influence of temperature, changing precipitation, and
extreme climatic events on soil organisms and greenhouse gas production. Mean-
while, indirect effects result from climate-driven changes in plant productivity
and species composition which alter soil physicochemical conditions, the supply of
carbon to soil and the structure and activity of microbial communities involved
in decomposition processes and carbon release from soil (Bardgett et al. 2008;
Fig. 2.19). Here, we consider direct effects of climate change on soil organisms and
biotic interactions, and how these can feed back greenhouse gases to the atmosphere
and contribute to global warming. Indirect effects of climate change on soil organ-
isms and biotic interactions which operate via changes in the plant community will be
discussed in Chapter 3.
One of the most commonly discussed contributions of soil organisms to climate
change is their role in soil organic matter decomposition and the notion that global
warming will accelerate rates of heterotrophic microbial activity, thereby increasing
the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved
organic carbon by hydrologic leaching (Jenkinson et al. 1991; Davidson and
Janssens, 2006). The concern here is that, because rates of soil respiration are more
sensitive than is primary production to temperature (Jenkinson et al. 1991; Schimel
et al. 1994), it is thought that climate warming will increase the net transfer of
carbon from soil to atmosphere, thus creating a positive feedback on climate change
 2.5 Biotic interaction and carbon dynamics • 53

CLIMATE CHANGE

Direct feedback Indirect feedback

Temperature Elevated CO2 CO2
Extreme events Temperature/precipitation

Autotrophic
Net primary respiration
production
Nutrient
cycle
feedback

Heterotrophic
Litter Rhizodeposits respiration

Microbial biomass
Soil fauna
DOC

SOIL ORGANIC MATTER

Fig. 2.19 Direct and indirect effects of climate change on soil microbial communities and
routes of feedback to global warming through carbon dioxide production. Direct effects include
the influence of temperature, changing precipitation, and extreme climatic events on soil
microbes and greenhouse gas production. Indirect effects result from climate-driven changes
in plant productivity and vegetation structure which alter soil physicochemical conditions, the
supply of carbon to soil and the structure and activity of microbial communities involved in
decomposition processes and carbon release from soil. DOC, dissolved organic carbon. From
Bardgett et al. (2008), with permission from Macmillan Publishers Ltd.

(Cox et al. 2000). Although it is well known that temperature is an important

determinant of rates of organic-matter decomposition, the nature of the relationship
between temperature and heterotrophic respiration, and its potential to feed back to
climate change, are far from clear (Davidson and Janssens 2006; Trumbore 2006).
There are several reasons for this uncertainty. First, soil organic matter is inher-
ently complex and the temperature dependence of decomposition of soil carbon
compounds of differing chemical composition and substrate quality vary substan-
tially (Davidson and Janssens 2006). For instance, some studies indicate that the
temperature sensitivity of litter decomposition increases as the quality of organic
54 • 2 Biotic interactions as ecosystem drivers

carbon consumed by microbes declines (Fierer et al. 2005; Conant et al. 2008).
Conversely, other studies report that the temperature sensitivity of more recalcitrant
substrates is similar (Fang et al. 2005; Conen et al. 2006) or less than (Luo et al. 2001;
Melillo et al. 2002; Rey and Jarvis 2006) that of more labile substrates. Second, there
is much potential for environmental constraints, such as physical and chemical
protection of organic matter, to decrease substrate availability for microbial attack,
and thereby dampen microbial responses to warming (Davidson and Janssens 2006).
As already discussed, faunal influences on decomposition processes vary regionally
depending on prevailing climatic conditions, suggesting that the sensitivity of de-
composition to climate change will likewise vary across biomes (Wall et al. 2008;
Powers et al. 2009). Third, there is much uncertainty about how reactive different
microbial and faunal groups and species are to temperature change. For instance,
several studies show a general lack of effects of elevated temperature on soil
communities (Hodkinson et al. 1996; Kandeler et al. 1998; Bardgett et al. 1999b),
and literature syntheses report only weak relationships between mean annual tem-
peratures and densities of soil faunal groups (Petersen and Luxton 1982; Wardle
2002) and microbial biomass (Wardle 1992). In contrast, other studies show that soil
organisms and the carbon-cycling processes that they drive are responsive to tem-
perature change. For instance, the abundance of enchytraeid worms which dominate
the fauna of acid and highly organic soils has been shown to be strongly related to
temperature. As such, it has been suggested that climate warming could increase their
abundance leading to enhanced carbon mineralization and carbon loss from soil
(Briones et al. 1998; Cole et al. 2002a, 2002b). Likewise, the abundance of soil
nematodes in the Dry Valleys of Antarctica, including the dominant species Scott-
nema lindsayae which plays a significant role in soil carbon cycling in these ecosys-
tems, has declined by over 40% in recent years due to declining air temperatures, with
possible implications for carbon dynamics (Fig. 2.20) (Barrett et al. 2004). Also,
even subtle warming (by 18C) has been found to cause a sustained increase in
ecosystem respiration rates in a sub-Arctic peatland, particularly in the subsurface
layers (25–50 cm depth), indicative of a large and long-lasting positive feedback
of carbon stored in northern peatlands to the global climate system (Dorrepaal
et al. 2009).
Further evidence of effects of climate change on decomposer communities arises
from studies on mushroom phenology. A recent analysis by Gange et al. (2007)
related temporal shifts in autumnal fruiting patterns of macrofungi in southern
England to shifts in climate and found that the average first-fruiting date of 315
species is now earlier, whereas last fruiting date is now later, than was the case
56 years ago. Their study also found that many species are now fruiting twice a year,
indicative of increased mycelial activity and possibly greater decomposition rates in
ecosystems. Similarity, a recent analysis of herbarium records over the period
1940–2006 in Norway found that the time of fruiting of mushrooms has changed
considerably over recent years, but in this case with an average delay in fruiting since
1980 of 12.9 days and with changes differing strongly according to taxa (Kauserud
et al. 2008). These changes in autumnal mushroom phenology coincide with the
 2.5 Biotic interaction and carbon dynamics • 55

(a) (b)

Fig. 2.20 Antarctic Dry Valleys (a) and the dominant species of nematode Scottnema lind-
sayae (b), which plays a significant role in soil carbon cycling in these ecosystems. Images by
Diana Wall (a) and M. Mundo (b).

extension of the growing season caused by global climate change and are likely to
continue under current climate change scenario (Kauserud et al. 2008). Finally, it is
uncertain as to whether short-term increases in carbon mineralization, which are
commonly observed in warming experiments in the field (Luo et al., 2001; Melillo
et al., 2002; Bradford et al. 2008), will be sustained due to depletion of substrate
availability and acclimation of soil communities to higher temperatures (Kirschbaum
2004; Bradford et al. 2008; but see Hartley et al. 2008). This level of uncertainty
about the response of soil organisms to climate change extends to unreliable model
predictions of soil carbon feedbacks to climate change (Kirschbaum 2006), and
resolving this issue represents a major research challenge for the future.
Climate-change-driven increases in the frequency of extreme weather events,
such as droughting and freezing, may have an even greater effect on soil organisms
and their activities than will overall changes in temperature and precipitation. For
instance, it is well known that both droughting and freezing have substantial direct
effects on microbial physiology and the composition of the soil microbial commu-
nity, with important consequences for ecosystem-level carbon dynamics (Schimel
et al. 2007). Further, the occurrence of soil surface ice layers, which are predicted to
become more frequent with climate change as a result of diminished snow cover, are
known to have strong negative effects on soil animals (Coulson et al. 2000) with
likely consequences for carbon and nutrient dynamics. However, the effects of
stressors resulting from climate change on soil biotic communities and the conse-
quences for carbon exchange are likely to vary substantially across ecosystems. For
instance, increased frequency and intensity of drought in drier ecosystems should
56 • 2 Biotic interactions as ecosystem drivers

result in moisture-limiting conditions for microbial activity, creating a negative

feedback on microbial decomposition and soil carbon loss from microbial respiration
(Nardo et al. 2004; Henry et al. 2005). Further, microbial responses to drying and
rewetting are likely to be less pronounced in soils that are frequently exposed to
natural drying/rewetting cycles (Birch 1958; Fierer and Schimel 2002). In contrast,
increased drought and drying in wetlands and peatlands, which will lower the water
table and introduce oxygen into previously anaerobic soil, will in turn create more
favourable conditions for microbial activity (Freeman et al. 2004a). Also, increas-
ing oxygen levels in previously anaerobic peatland soils has been shown to enhance
the activity of phenol oxidases which play a pivotal role in the breakdown of
recalcitrant organic matter (Freeman et al. 2004a; Zibilske and Bradford 2007).
Because peatlands and wetlands represent among the largest stocks of terrestrial
carbon globally (Ward et al. 2007), such enhanced breakdown of recalcitrant organic
matter under drying could have major implications for the global carbon cycle
(Freeman et al. 2004a). Before leaving this topic, it is important to note that
methanogenic pathways are also affected by increased oxygen availability associated
with drought, in that methane emissions are reduced by toxic effects of oxygen on
methanogens (Roulet and Moore 1995; Freeman et al. 2002). Also, drought can have
marked effects on nitrous oxide emission from soils, a potent greenhouse gas that is
increasing in atmospheric concentrations at the rate of 0.2–0.3% per year (Houghton
et al. 1996). However, responses depend on the severity of drought, in that modest
summer drought is likely to have limited effect on soil nitrous oxide emissions,
whereas more extreme drought can greatly increase them (Dowrick et al. 1999).
Another climate-change-related factor that is likely to have a profound influence on
soil communities and decomposition in Arctic and alpine regions is reduced snow
cover and the thawing of permafrost. It has been estimated that 25% of Earth’s
permafrost could thaw by 2100 due to climate warming, exposing considerable
amounts of otherwise protected organic matter to microbial decomposition (Anisimov
et al. 1999), thus creating a positive feedback on climate change (Davidson and
Janssens 2006; Heimann and Reichstein 2008). Consistent with this, Schuur et al.
(2009) found that permafrost thaw over decadal timescales in an Alaskan tundra
landscape has caused significant losses of soil carbon, despite increased plant growth
and ecosystem carbon input. Because snow is an important insulator of winter soil
biological processes, predicted reductions in snow cover in alpine and Arctic regions
should also increase soil freezing, with consequences for root mortality, nutrient
cycling, and microbial-driven soil processes (Groffman et al. 2001; Bardgett et al.
2005). Strong microbial responses to freeze–thaw cycles have been shown in several
studies, leading to increased microbial activity and greenhouse gas emission
(Christensen and Tiedje 1990; Sharma et al. 2006), altered microbial substrate use
(Schimel and Mikan 2005) and the expression of denitrifying genes leading to the
release of nitrous oxide gas (Sharma et al., 2006). However, a recent synthesis of
literature on this topic concluded that while freeze–thaw events might induce gaseous
and/or solute losses of nitrogen from soils that are relevant at an annual time scale,
they may have little effect on (or even reduce) soil carbon losses relative to unfrozen
 2.5 Biotic interaction and carbon dynamics • 57

conditions in the longer term (Matzner and Borken 2008). Further, recent studies in
subalpine forest in Colorado indicate that reduced snow cover can suppress rates of
soil respiration through impairing a unique and highly temperature-sensitive soil
microbial community that occurs beneath snow (Monson et al. 2006); this may
significantly affect winter soil microbial activity, carbon storage, and carbon dioxide
efflux in alpine and Arctic regions.

2.5.3 Multiple global change drivers and soil biotic interactions

The majority of studies to date that have explored effects of climate change on
biological systems and soil organisms have considered single factors, such as ele-
vated atmospheric carbon dioxide concentration, warming, and drought. However,
there is much potential for interactions between these factors to have additive or
antagonistic effects on soil organisms and the activities that they drive (Shaw et al.
2002; Mikkelsen et al. 2008; Bardgett et al. 2008; Tylianakis et al. 2008). Very little
is known about the influence of multiple and interacting climate drivers on soil
organisms and their activities, although some studies do point to strong non-additive
belowground effects of these drivers, with feedback consequences for carbon
exchange. For instance, microbial decomposition of peat was found to be signifi-
cantly greater when subject to both elevated temperature and atmospheric carbon
dioxide than when these factors were each elevated singly (Fenner et al. 2007a,
2007b). This created an even stronger positive feedback on carbon loss from soil as
dissolved organic carbon in drainage water and respiration (Freeman et al. 2004b).
Added to this complexity is our knowledge that other organisms and trophic groups
that influence soil microbes directly, such as microbial-feeding fauna, will also
respond to multiple climate change factors (Wardle 2002; Bardgett 2005; Tylianakis
et al. 2008). This complexity further hampers our ability to predict effects of multiple
climate change drivers on soil biological communities and carbon-exchange
feedbacks.
In addition to multiple climate change drivers, soil organisms and their activities
are also affected substantially by other global change phenomena, such as nitrogen
deposition, invasion of new species, and land-use change. Perhaps the strongest
driver is land-use change (see Sala et al. 2000), and it is widely documented that
changes in the intensity of land use or the conversion of natural vegetation to
agriculture or forestry can have substantial, and often strongly negative and irrevers-
ible, effects on soil biological communities and their activities (Brussaard et al. 1997;
Wardle 2002; Bardgett 2005). One pattern that commonly emerges in the context
of land-use change is that intensification of farming, including increased tillage,
fertilizer use, and grazing, is typically associated with an increased role of the
bacterial-based energy channel relative to the fungal-based channel (Hendrix et al.
1986; Wardle 2002; Bardgett 2005). As discussed above, this increased bacterial role
is associated with faster, leakier nutrient cycling and more losses of nutrients and
carbon in water and greenhouse gases to the atmosphere (Wardle et al. 2004a; Van
der Heijden et al. 2008). In contrast, low-intensity management systems often
58 • 2 Biotic interactions as ecosystem drivers

encourage fungal-based soil food webs that are more similar to those of natural
systems, and tend to be associated with more efficient nutrient cycling (Bardgett
and McAlister 1999; de Vries et al. 2006; Gordon et al. 2008) and enhanced soil
carbon sequestration (Six et al. 2006; De Deyn et al. 2008).
Soil biological communities are also strongly affected by nitrogen enrichment,
which is of high relevance because anthropogenic activities have substantially in-
creased global rates of nitrogen fixation and deposition (Vitousek et al. 1997a;
Holland et al. 1999; Bobbink and Lamers 2002; Galloway et al. 2008). For instance,
it is well known that nitrogen enrichment can have direct and differential impacts on
extracellular enzymes involved in decomposition processes. This typically involves
stimulation of the synthesis of cellulases which degrade labile, high-cellulose litter,
but suppression of the synthesis of ligninolytic enzymes by white rot fungi which
decompose recalcitrant, high-lignin litter (Carreiro et al. 2000; Frey et al. 2004;
Waldrop et al. 2004; Allison et al. 2008). Also, nitrogen deposition is known to
influence the abundance and diversity of different components of the soil microbial
community. These include bacteria, saprophytic fungi (Donnison et al. 2000;
Bardgett et al., 2006; Allison et al. 2008), mycorrhizal fungi (Egerton-Warburton
and Allen 2000; Frey et al. 2004), and soil fauna (Scheu and Schaefer 1998; Ettema
et al. 1999), which are also affected by climate change and are well known to have
substantial effects on decomposition processes and ecosystem-level carbon ex-
change. A recent meta-analysis on this topic revealed that soil microbial biomass
declined 15% on average under nitrogen fertilization, but that declines in abundance
of microbes and fungi were more evident in studies of longer durations and with
higher total amounts of nitrogen added (Treseder 2008). Moreover, that study showed
negative responses of microbial biomass to nitrogen fertilization to be significantly
correlated with declines in soil carbon dioxide emissions, indicating that moderate
declines in microbial biomass under nitrogen fertilization may also have conse-
quences for carbon fluxes. However, another meta-analysis of 109 studies across
the globe revealed that nitrogen enrichment had no significant effect on net ecosystem
carbon dioxide exchange in non-forest natural ecosystems, but did increase methane
and nitrous oxide emissions by 97 and 216%, respectively (Liu and Greaver 2009). It
was suggested, therefore, that any potential positive effects of nitrogen enrichment on
the global terrestrial carbon sink should be offset by the stimulation of methane and
nitrous oxide emissions, which are more potent greenhouse gases than is carbon
dioxide (Liu and Greaver 2009). Importantly, and as will be considered in Chapter 3,
nitrogen deposition and other global changes can also influence soil microbes and
decomposition processes indirectly through altering vegetation composition and
productivity, and by alleviating progressive nitrogen limitation of plant growth,
which typically occurs under elevated atmospheric carbon dioxide (Finzi et al.
2002; Luo et al. 2004; de Graaff et al. 2006).
In general, very little is known about the combined effects of global changes on
soil biological communities and their activities, but they clearly have the potential to
amplify, suppress or perhaps even neutralize climate-change-driven effects on soil
microbes and their feedback to carbon exchange (Bardgett et al. 2008). A recent
 2.6 Conclusions • 59

synthesis (Tylianakis et al. 2008) of data from 688 published studies on the effects of
global change on biotic interactions in terrestrial ecosystems (including those that
occur in the decomposer food web) highlighted that there is substantial variability
among studies in both the magnitude and direction of effects of any given global
change driver on any given type of biotic interaction. Further, that analysis high-
lighted that the unanticipated effects of multiple drivers acting simultaneously create
major challenges in predicting future responses to global environmental change.
Experimental studies that simultaneously vary two or more global change drivers
within the same experiment therefore have considerable promise for improving our
understanding of how interactions involving soil communities and their effects on
ecosystem-level processes may respond to current global change scenarios.

2.6 Conclusions
In this chapter, we have explored how the activities and interactions of belowground
communities regulate belowground processes, and the consequences of this for the
productivity, diversity, and composition of plant communities. We have also dis-
cussed the role of soil biotic interactions in a global change context, focusing on their
influence on ecosystem carbon dynamics and contribution to climate change through
carbon-cycle feedbacks. While it has long been recognized that soil microorganisms
play a pivotal role in the breakdown of organic matter, and liberation of plant growth-
limiting nutrients, the last decade has seen several significant advances in this area.
For instance, recent recognition of the importance of direct uptake of organic nitrogen
by plants has led to a radical rethink of terrestrial nitrogen cycling and in particular of
the microbial processes that control plant nitrogen availability (Schimel and Bennett
2004; Jones et al. 2005). We also have greater awareness that the cycling of labile
nitrogen pools relies on intimate, temporal coupling between plants and microbes and
their seasonal resource demands (Jaeger et al. 1999; Bardgett et al. 2005). Further, we
now recognize that partitioning of nitrogen (and possibly phosphorus) on the basis of
chemical form can provide a mechanism for plants to efficiently partition a limited
soil nutrient pool, thereby facilitating species coexistence and the maintenance of
plant diversity (McKane et al. 2002; Kahmen et al. 2006; but see Harrison et al.
2007). Recent years have also witnessed a growing understanding of the mechanisms
by which mycorrhizal fungi contribute to plant community dynamics, for instance by
promoting more efficient exploitation and equitable distribution of nutrients within
the plant community (Van der Heijden et al. 1998; Maherali and Klironomos 2007),
and of the evolutionary mechanisms that explain why certain types of ecosystems
lack symbiotic nitrogen-fixers and therefore experience greater nitrogen limitation
(Menge et al. 2008). Despite these advances, the contribution of soil microbes to
ecosystem functioning is still poorly understood, largely because over 95% of
microbes are unable to be cultured on conventional media (Van der Heijden et al.
2008). Recent advances in ecological genomics and the use of microarrays to detect
key genes responsible for key ecosystem processes (Van Straalen and Roelofs 2006;
60 • 2 Biotic interactions as ecosystem drivers

Zak et al. 2006; He et al. 2007) offer potential to overcome this problem and improve
understanding of the roles that soil microbes play in regulating nutrient and plant
community dynamics (Van der Heijden et al. 2008).
While plant nutrient availability is strongly regulated by microbial activities, the
soil also hosts an abundant and highly complex community of invertebrates which
derive most of their nutrition and carbon either directly from roots and exudates, or
indirectly from feeding on microbes (Pollierer et al. 2007). There is ample evidence
that faunal consumers of microbes and their predators strongly regulate nutrient and
plant community dynamics by altering the balance between microbial immobilization
and mineralization, and hence nutrient availability (Wardle 2002; Bardgett 2005).
Moreover, there is greater recent recognition that larger fauna such as ecosystem
engineers can substantially modify soil processes and the temporal and spatial
dynamics of plant communities through several mechanisms including alteration of
the physical structure of soil, transportation of faecal material and propagules, and
influencing the movement of water and soluble nutrients (Lavelle et al. 1997;
Bardgett et al. 2001a). Another important development is the recognition that nutrient
availability to plants can also be controlled several trophic steps away from the plant
root through top-down control (Moore et al. 2003). This indicates that an under-
standing of how belowground communities influence aboveground community prop-
erties requires explicit consideration of the role of predation as a control point in
belowground processes (Moore et al. 2003). A further development in this area is the
recognition that compositional changes in the soil food web, including broad shifts
between fungal and bacterial-based energy channels, have important consequences
for ecosystem processes of decomposition and nutrient cycling (Wardle et al. 2004a;
Van der Heijden et al. 2008). However, it is also evident that understanding the
functional consequences of changes in soil food web composition also requires
recognition of how individual species contribute to multiple species interactions
(Heemsbergen et al. 2004) and of environmental context. This latter point is espe-
cially important given that the role of soil biotic interactions relative to abiotic factors
in regulating ecosystem processes varies tremendously under different environmental
conditions and across biomes (Gonzalez and Seastedt 2001; Wall et al. 2008).
A topic that has attracted much recent attention is the role that soil organisms and
biotic interactions play in regulating carbon dynamics in terrestrial ecosystems,
especially in the context of land–atmosphere exchanges of carbon and carbon-cycle
feedbacks that could amplify climate change. One key development is the increased
recognition that recent plant photosynthate acts as a major driver of soil biological
activity and carbon flux in terrestrial ecosystems, accounting for as much as half of
the respiratory carbon release from soil (Högberg et al. 2001; Steinmann et al. 2004;
Pollierer et al. 2007). However, much remains to be learned about the mechanisms
that govern respiratory fluxes from soil, especially in the context of climate change
which can affect soil organisms and their activities directly via changes in tempera-
ture and precipitation, and indirectly via changes in vegetation and photosynthate
supply (Bardgett et al. 2008). For instance, although it is well established that tem-
perature acts as an important determinant of the rate of organic matter decomposition,
 2.6 Conclusions • 61

and recent evidence points to warming and permafrost thaw causing sustained loss of
carbon from tundra soils (Schuur et al. 2009; Dorrepaal et al. 2009), the nature of
the relationship between temperature and heterotrophic microbial respiration and its
potential to feed back to climate change is unclear (Davidson and Janssens 2006;
Trumbore 2006). Also, while there is mounting evidence that decomposer organisms
and their activities are strongly affected by extreme events associated with climate
change (Schimel et al. 2007), the consequences of this for decomposition processes and
carbon exchange remain little understood. This level of uncertainty about the response
of soil organisms and their activities to climate change extends to unreliable model
predictions of soil carbon feedbacks (Kirschbaum 2006), and resolving this issue
represents a major research challenge for the future.
Finally, we highlight that global change drivers other than climate change also
have strong effects on soil organisms and their activities, and that these effects often
have far-reaching consequences for ecosystem-level properties, including soil carbon
sequestration. However, it is becoming increasingly apparent that our ability to
predict future responses to global change, and the potential for climate-change
mitigation through carbon sequestration, requires a greater understanding of the
simultaneous effects of multiple global change drivers on soil biological communities
(Tylianakis et al. 2008; Bardgett et al. 2008). As highlighted in this chapter, very little
is known about this, although there is clearly much potential for interactions between
global change drivers to amplify, suppress, or even neutralize climate change driven
effects on soil microbes and their feedback to carbon exchange (Bardgett et al. 2008).
As will also be argued in Chapter 3, the unanticipated effect on soil biological
communities of multiple drivers acting simultaneously represents a major research
challenge for the future.
3
Plant community influences
on the soil community and
plant–soil feedbacks

3.1 Introduction
The community structure of plants and that of soil organisms are coupled to one
another to varying degrees. In Chapter 2, we described how communities of soil
organisms could influence the productivity and composition of plant communities
through a variety of mechanisms. In turn, plants serve as determinants of soil com-
munities. This may happen through either the indirect or direct pathways highlighted
in Chapter 2 (Fig. 2.1): the indirect pathway involves plants influencing organisms in
the decomposer food web by determining the quantity and quality of litter that enters
the soil, whereas the direct pathway involves the characteristics of live roots deter-
mining the accessibility of root-associated organisms to the resources produced by the
roots. While the indirect pathway usually involves a relatively low level of specificity
between plants and soil organisms, there is increasing recognition that the direct
pathway often involves a high level of specificity among aboveground and below-
ground taxa (Wardle et al. 2004a). Further, there is growing recognition that the effects
of plants and soil organisms on one another results in important feedback mechanisms
between the aboveground and belowground biota (Van der Putten et al. 1993;
Bever et al. 1997; Wolfe and Klironomos 2005; Kulmatiski et al. 2008).
Since the early 1990s, the issue of how plant species may drive ecosystem
processes, including those driven by soil organisms, has attracted considerable
attention from ecologists (e.g. Hobbie 1992; Lawton 1994). However, it is important
to recognize that this issue has a strong historical basis. For example, the mull and
mor theory of Müller (1884) explicitly recognizes the role that plant species, and
variation within plant species, can have in determining the community composition
of soil fauna, as well as feedbacks through effects on nutrient supply from the soil.
Subsequently, Handley (1954, 1961) showed through a series of experiments in the
UK that Calluna vulgaris differed from coexisting plant species because it could
produce tannin–protein complexes that inhibited mineralization of nitrogen, and
therefore the nutrition of coexisting plant species. Furthermore, the effect of plant
species on those soil organisms intimately associated with plant roots has long been
recognized by agronomists. For example, crop rotations have long been used by
farmers to prevent specific crop species from accumulating soil-borne pathogens that
 3.2 Plants and the belowground subsystem • 63

in turn would impair productivity of that crop through negative feedback. Further, as
noted in Chapter 2, farmers have also recognized for centuries that utilizing plant
species mixtures that include legumes which support nitrogen-fixing bacteria can
greatly enhance soil fertility and crop nutrition.
To understand how plant communities influence soil communities, it is first
necessary to understand how and why different species in a plant community vary
in their belowground effects. Plant communities usually consist of several coexisting
species that differ in their ecophysiological characteristics, and the literature is replete
with examples of how different plant species vary in their effects on soil communities
and processes. As such, comparisons of highly contrasting species in the same plant
community provide compelling evidence that interspecific variation in litter quality is
a powerful determinant of plant litter decomposition and the availability of nutrients
required for plant growth (e.g. Berendse 1998; Bowman et al. 2004; Santiago 2007).
Similarly, coexisting species can differ greatly in their rhizosphere communities of
both microbes (Aberdeen 1956; Grayston et al. 1998) and microbe-feeding fauna
(De Deyn et al. 2004; Viketoft 2008). The functional characteristics of plant species
also determine the communities of those organisms that interact more directly with
plant roots, such as root pathogens (Korthals et al. 2001) and mycorrhizal fungi
(Cornelissen et al. 2001a). While the observation that plant species differ in the
communities of soil organisms that they support is perhaps unsurprising, understand-
ing the mechanistic basis of these species effects and their implications for ecosystem
processes is essential for understanding the functioning of terrestrial ecosystems.
The goal of this chapter is to provide an outline of how plant community charac-
teristics influence the soil biological community and thereby affect ecosystem pro-
cesses and properties. In doing this, we first outline how variation among and within
plant species influences soil communities and thereby the biogeochemical processes
that they drive. We also consider the overarching effect of plant attributes or traits in
governing these effects. Based on this framework, we then consider aboveground–
belowground feedbacks in the context of vegetation succession and ecosystem
development, and finally in the context of shifts in vegetation composition brought
about by human-induced global change. In Chapter 2, we considered the effects of the
belowground subsystem on the aboveground subsystem; our ultimate goal in this
chapter is to complement Chapter 2 by highlighting how aboveground and below-
ground communities can operate in tandem to drive community and ecosystem
properties.

3.2 How plants affect the belowground subsystem

3.2.1 Differential effects of different plant species
Within the soil food web, any given group of organisms is likely to be strongly
affected by differences among plant species only if it is driven primarily by bottom-up
control (i.e. resource quantity and quality) rather than by top-down control (i.e. regulation
64 • 3 Plant influences and plant–soil feedbacks

by its predators) or by abiotic factors. As discussed in Chapter 2, the importance of

top-down and bottom-up regulation in the soil food web differs among major food web
components, as well as within major groups under differing environmental conditions
(Bengtsson et al. 1995; Mikola and Setälä 1998b; Wardle 2002; Moore et al. 2003).
As a consequence, variable effects of plant species on soil taxa and food-web groups may
be expected.
One mechanism through which different plant species may vary in their effects on
soil food web biota is through differences in net primary production (NPP); that is,
the quantity and quality of resources that they return to the soil as plant litter and
rhizodeposits. However, effects of NPP on components of the soil food web are far
from consistent, and different studies that have investigated how components of the
soil food web vary across gradients of NPP have found somewhat contrasting results:
responses can be positive, neutral, or even negative depending on environmental
context (Fig. 3.1). In this light, it is perhaps unsurprising that experimental studies
which compare planted monocultures of several plant species do not necessarily find
the most productive plant species to support the greatest density or biomass of soil
organisms. For example, in monoculture plots of each of eight grass and forb species,
De Deyn et al. (2004) found little relationship between plant shoot mass and
abundance of soil nematodes, including those involved in the decomposer food
web as well as those that function as root herbivores. Similarly, Hooper and Vitousek
(1997, 1998) did not find the most productive monocultures of plant functional
groups in serpentine grassland to necessarily support higher levels of soil microbial
biomass. Further, Wardle et al. (2003d) found for monocultures of nine herbaceous
plant species that while the biomass of the basal trophic level of the soil food web (i.e.
the microflora) was generally greatest for the most productive plant species, this
pattern was not generally apparent for the higher consumer trophic levels.
Bottom-up effects of plant species differences on soil food-web groups and the
belowground processes that they drive are, however, apparent from the large number
of studies that have considered interspecific differences in litter quality. There is a
vast literature showing that differences in litter chemical constituents between differ-
ent plant species (e.g. nitrogen, phosphorus, polyphenolics, lignin, soluble carbon,
calcium) drives litter decomposition rates, and therefore the activity of decomposer
organisms (Swift et al. 1979; Berg and McClaugherty 2003). This is consistent with
studies showing that species that produce high-quality (i.e. rapidly decomposing)
litter support greater densities or biomasses of litter-decomposer microflora and fauna
(e.g. Parmelee et al. 1989; Hansen 2000), and greater litter-consumption rates by
saprophagous fauna such as arthropods (Nicolai 1988) and earthworms (Hobbie et al.
2006). Litter-quality differences among plant species may also serve as powerful
determinants of the community structure of both decomposer microflora (Widden and
Hsu 1987) and fauna (Wardle et al. 2006) inhabiting the litter. Further, there is some
evidence that some plant species can preferentially select for decomposer taxa that
enhance the decomposition of their own litter (e.g. Hansen 1999; Negrete-Yankele-
vich et al. 2008; Vivanco and Austin 2008; Ayres et al. 2009), indicative of feedback
mechanisms that will be discussed later in this chapter.
 3.2 Plants and the belowground subsystem • 65

(a) (b)
200
R 2 = 0.512 35 R 2 = 0.394
Microbial biomass

P < 0.01 P < 0.001

Sustrate-induced

(μg CO2-C/h/g)
150 30

respiration
(g/m2)

100 25

50 20

0 0
0 500 1000 1500 20 40 60 80
Primary productivity Primary productivity
2/week)
(g/m2/year) (g/m

(c) (d)
1500
300 R 2 = 0.592 R 2 = 0.668
Microbial biomass

P < 0.01 P < 0.024

Microbial biomass

200 1000
(μg C/g)
(μg C/g)

100 500

0
0
0 100 200 300 0 1000 2000
Crop yield (g/m2) Primary productivity
(g/m2/year)

(e) (f)

R 2 = 0.504 R 2 = 0.774
4 P < 0.05 40 P < 0.05
(thousands/m2)
(millions/m2)

Nematodes
Nematodes

2 20

0 0
0 10 20 0 10 20
Primary productivity Primary productivity
(kg/ha/year) (relative)

Fig. 3.1 Biomass or populations of consumer organisms in the decomposer food web in
response to gradients of NPP. Consumer organisms considered are: (a) soil microbial biomass
in late successional North American forests (Zak et al. 1994); (b) substrate-induced respiration
(relative measure of microbial biomass) in a New Zealand grassland (Wardle et al. 1995);
(c) soil microbial biomass in cropping fields in Alabama, USA (Insam et al. 1991); (d) soil
microbial biomass in coniferous forests in Oregon, USA (Myrold et al. 1989); (e) soil nematode
populations in a New Zealand grassland (Yeates 1979); (f) soil nematode populations in
Japanese forests (Kitazawa in Yeates 1979). Derived from Wardle (2002).
66 • 3 Plant influences and plant–soil feedbacks

Plant species that vary greatly in their litter quality also often differ in the rates of
processes that occur in their underlying soil (Binkley and Giardina 1998). This is
especially apparent for comparisons of coexisting plant species that have vastly
differing litter properties (Fig. 3.2). For example, in Dutch moist heathlands, the
grass Molinia caerulea produces litter of a much higher quality (i.e. higher nitrogen,
lower lignin) than does the coexisting dwarf shrub Erica tetralix. Consequently, rates
of microbially driven processes, such as nitrogen mineralization, are much greater
in soil under Molinia than beneath Erica (Berendse 1998). Likewise, Empetrum

(a) (b)

(c) (d)

Fig. 3.2 Pairs of co-occurring plant species that have vastly contrasting effects on belowground
organisms and processes. (a) Empetrum hermaphroditum and (b) Deschampsia flexuosa from
the northern Swedish boreal zone. Empetrum is a slow-growing species with long-lived leaves
that produces poor-quality litter containing high concentrations of lignin and the stilbene
phenolic batatasin III which adversely affects a range of aboveground and belowground
processes and organisms. In contrast the grass Deschampsia is a fast-growing species that has
a rapid turnover of tissue and that produces high-quality poorly defended litter with low levels of
lignin and phenolics (see Nilsson et al. 2002). (c) Erica tetralix with Narthecium ossifragum and
(d) Molinia caerulea in Dutch moist heathlands. Erica grows slowly and produces well-
defended poor-quality litter with a high lignin concentration that only slowly releases mineral
nitrogen, while Molinia produces high-quality litter and promotes nitrogen mineralization (see
Berendse 1998). Disturbance and addition of fertilizers can result in a switch from domination
by Empetrum to domination by Deschampsia in northern Sweden, and from Erica to Molinia in
Dutch heathlands. Photo credits: (a, b) M.-C. Nilsson; (c, d) J. Janssen.
 3.2 Plants and the belowground subsystem • 67

hermaphroditum in the northern Swedish boreal forest produces litter of poor quality
with high concentrations of the stilbene phenolic batatasin III, which impairs soil
microbial biomass and activity, and litter-decomposition rates relative to litter from
coexisting plant species such as Vaccinium myrtillus and Deschampsia flexuosa
(Nilsson and Wardle 2005). Further, in alpine grasslands in Colorado, the forb
Geum (formerly Acomastylis) rossii produces shoot and root litter with a high
concentration of labile polyphenolics, while the coexisting and fast-growing grass
Deschampsia caespitosa does not. These phenolics appear to be readily utilized by
the soil microflora, leading to greater microbial biomass and promotion of microbial
immobilization of nitrogen, which reduces nitrogen availability to D. caespitosa,
thereby reducing its growth (Bowman et al. 2004; Meier et al. 2008).
Plant species also differ greatly in the resources that they contain in their roots and
release through the rhizosphere. It is well established that plant species vary greatly in
their effects on those soil organisms that are intimately associated with their roots, and
that there is a high degree of specificity between plant species and taxa of ectomycor-
rhizal fungi (Smith and Read 1997), arbuscular mycorrhizal fungi (Van der Heijden
et al. 1998a), and root pathogens and herbivores (Yeates 1979; Korthals et al. 2001).
However, as mentioned in Chapter 2, plants can also exert important effects on
decomposer organisms through recently fixed carbon released into the soil from the
plant root system. This has long been known to be important in plant communities
dominated by fast-growing herbaceous species such as grasslands. For instance, root
systems of different herbaceous plant species are known to vary greatly in the densities
and community composition of the bacteria, fungi, and microfauna that they support
(Rovira et al. 1974; Grayston et al. 1998; Bardgett et al. 1999c), and live roots of
different plant species can differ greatly in their effects on microbial activity and
decomposition processes (Dormaar 1990). As shown by Van der Krift et al. (2002),
live roots of four grass species differed greatly in their effects on decomposition of dead
root material, with live roots of Festuca ovina having especially strong positive effects,
probably because this species exuded high amounts of compounds that stimulate
microbial activity. Likewise, the above-mentioned slow-growing alpine forb G. rossii
has recently been shown to produce phenolic-rich rhizodeposits which strongly influ-
ence microbial community dynamics and soil nutrient availability, with consequences
for the growth of the coexisting grass D. caespitosa (Meier et al. 2008, 2009).
As noted in Chapter 2, there is also recent evidence from experiments in forests that
have utilized C-13 enrichment labelling (Pollierer et al. 2007; Högberg et al. 2008)
and tree girdling (Högberg et al. 2001) to show that tree roots release substantial
quantities of recently fixed carbon to the belowground subsystem, and that this can
serve as a major driver of soil respiration, mycorrhizal fungal production (Högberg
et al. 2001), saprophytic microflora (Högberg et al. 2008), and soil invertebrate
communities (Pollierer et al. 2007). Although to date studies of this type have been
performed on single tree species, it is plausible that these short-term allocation
patterns may vary greatly among coexisting tree species, thus serving as an important
mechanism by which differences among tree species effects are manifested below-
ground. Testing of this hypothesis, however, remains to be performed.
68 • 3 Plant influences and plant–soil feedbacks

3.2.2 Effects of within-species variation

Although most work on how different plants affect belowground organisms and
processes has been at the across-species level, there is increasing recognition that
variability at the within-species level may also be an important ecosystem driver.
Many studies have shown that measures of leaf litter quality, decomposition,
and nutrient mineralization can vary within species across environmental gradients
(e.g. Crews et al. 1995; Northup et al. 1995) or among individuals or groups of
individuals of a single species (e.g. Madritch and Hunter 2002). Such studies
highlight the magnitude and ecological significance of phenotypic variability that
can exist at the within-species level. However, it is only relatively recently that the
importance of within-species variability at the genetic level has become appreciated
as an important ecological driver (Bailey et al. 2009).
A small but growing number of studies have characterized plant genetic variability
within species or within hybrid swarms, and related this variability to effects of the
plant on belowground organisms or processes (Fig. 3.3). For example, Treseder and
Vitousek (2001) grew seedlings of Metrosideros polymorpha collected from each of
three sites in Hawai’i varying in nutrient limitation in a common garden experiment.
They found that plants from the three sites were genetically distinct, and that they
differed in nutrient-resorption potential, concentrations of litter lignin and nitrogen,
and litter decomposability. Schweitzer et al. (2004) similarly utilized a common
garden experiment to show that concentrations of condensed leaf tannins varied
greatly among hybrids of Populus fremontii  Populus angustifolia, and that this
was in turn closely related to variability among the hybrids in litter decomposability
and rates of soil nitrogen mineralization. Subsequent work on that experiment
revealed strong linkages between plant genotype and both microbial biomass and
microbial community structure (Schweitzer et al. 2008). Studies by Classen et al.
(2007) on Pinus edulis revealed that strains that differed in their level of herbivore
resistance also differed in the rate of shoot and root litter decomposition and nutrient
release. Similarly, Silfver et al. (2007) utilized a common garden experiment to show
that Betula pendula genotypes which differed in their herbivore resistance also
differed in their foliar nitrogen and protein concentrations, as well as in their litter
decomposability. With regard to decomposer biota, Crutsinger et al. (2008) found
that plots planted with different genotypes of Solidago altissima sometimes also
supported different densities of litter-dwelling microarthropods. Collectively, these
studies point to wide ranging effects of genotypes on the belowground subsystem,
although the magnitude of these within-species effects relative to that for across-
species effects remains mostly unexplored.
Those studies that have explored belowground consequences of within-species
genetic variability serve to highlight the linkage between community genetics and
ecosystem processes. As such they have contributed to the development of the
concept of the ‘extended phenotype’ (sensu Whitham et al. 2003) in which plant
genetics at the within-species level drives community properties and ecosystem
functioning. Recent work has also highlighted that the potential of plant genes to
 (a)
1.0

0.9

Decay constant (year−1)

0.8

0.7

0.6

0.5

0.4

0.3

0 20 40 60 80 100 120
Condensed tannin: nitrogen ratio
(b)
48
(% mass loss within 3 months)
Litter decomposition

44

40

36

32

2 5 17 25 4 15 8 3 22 18 30 9 24 26 19 20 6 12 16
Genotype ID
(c)
8
Colembola
Abundance
No. of species or individuals

6 Richness

0
4 5 14 17 19 20 22 24 25 26 27 28
Genotype ID

Fig. 3.3 Examples of the magnitude of effects of genetic variability on belowground processes
and organisms. (a) Litter decay rates and condensed-tannin-to-nitrogen ratios for Populus fre-
momtii, Populus angustifolia, and their hybrids. From Schweitzer et al. (2004), with permission
from Wiley Blackwell; (b) mean mass loss (+1 SE) of decomposing litter for each of 19 genotypes
of Betula pendula in a common garden experiment. From Silfver et al. (2007), with permission
from Springer ScienceþBusiness Media; (c) litter-dwelling collembolan abundance and species
richness (mean +1 SE) in plots planted with each of 12 genotypes of Solidago altissima. From
Crutsinger et al. (2008), with permission from Springer ScienceþBusiness Media.
70 • 3 Plant influences and plant–soil feedbacks

influence soil microbial communities and the processes that they drive is able to be
inherited by subsequent plant generations, indicative of ‘community heritability’
(Schweitzer et al. 2008; Whitham et al. 2003, 2008). So far, the evolutionary
implications of this heritability are unclear, and it is not known whether plant
genotypes derive a selective advantage through it. Nevertheless, the concept of
community heritability has considerable potential for the integration of genetic
characteristics at the plant level with feedbacks between the producer and decom-
poser subsystems.

3.2.3 Spatial and temporal variability

There is increasing recognition that, within plant communities, soil organisms and the
processes that they drive can vary greatly in both space and time (Ettema and Wardle
2002; Bardgett et al. 2005; Berg and Bengtsson 2007). This is determined in a large part
by the spatial and temporal variability of resources produced by the plant, especially
when the soil biota is strongly driven by bottom-up forces. The spatial and temporal
effect of plants on the belowground subsystem has the potential to operate as an
important driver of the release and supply of nutrients required for plant growth.
Spatial patterning of soil biota can occur both vertically and horizontally (Berg and
Bengtsson 2007); here we focus on the latter as this is more likely to be driven by
plant species effects. Spatially explicit approaches for studying soil organisms and
processes have revealed patterns of spatial patterning ranging from millimetres to
hundreds of metres, meaning that patterning exists in a nested manner across a wide
range of scales (Ettema and Wardle 2002) (Fig. 3.4). Plants influence these spatial

Environmental factors Disturbance Population processes

Fine-scale effects
Reproduction
of roots, organic
Mortality
particles, and
Active dispersal
soil structure
Crytobiosis
Plot-to fieldscale Competition
effects of burrowing Predation
animals, individual Mutualism
plants, and plant
communities Passive
dispersal
Large-scale gradients
of texture, soil carbon,
topography, and
vegetation systems

Fig. 3.4 Determinants of spatial heterogeneity of soil organisms. Spatial heterogeneity of soil
organisms and processes is distributed on nested scales, and is driven by both biotic and abiotic
factors including the effects of plant species. From Ettema and Wardle (2002), with permission
from Elsevier.
 3.2 Plants and the belowground subsystem • 71

patterns at several of these scales, suggesting that differences among plant species are
important drivers of the spatial structure of the belowground subsystem. For example,
a spatially explicit approach was used by Grundmann and Debouzie (2000) to show
that bacteria capable of oxidizing ammonium and nitrate were aggregated over the
order of millimetres, apparently reflecting the spatial distribution of fine roots.
Meanwhile, Wachinger et al. (2000) found that spatial heterogeneity of methanogenic
bacteria was related to small-scale patchiness of plant litter. At larger scales, spatial
patterning of soil organisms is well known to be reflective of the spatial patterning of
plants (Klironomos et al. 1999; Wardle 2002).
The role of plant species effects in driving soil processes is most apparent when
plant species of contrasting ecology occur together in the landscape, but are
spatially segregated from one another. In these cases each plant can directly
influence the soil under it, and when horizontal transport rates of plant-derived
resources are low this creates a spatial mosaic of soil biota and the processes that
they drive. This is especially apparent when individuals of woody plant species
(trees and shrubs) are scattered through the landscape, yielding island-like effects
in which soil organism densities and soil processes are greatly altered relative to
the rest of the landscape. Examples of this phenomenon include individual shrubs
in arid ecosystems that create ‘islands of fertility’ (e.g. Schlesinger and Pilmanis
1998), and ‘tree islands’ following krummholz formation in alpine tundra above
the treeline (Seastedt and Adams 2001). Coexisting tree species that produce
resources of greatly contrasting quality also influence the spatial patterning of
soil organisms and processes. For example, spatial distribution of the soil microbial
community in a Swedish boreal forest was found by Saetre and Bååth (2000) to be
determined by the spatial arrangement of the two dominant tree species, the
deciduous Betuna pendula and the evergreen Picea abies. This type of phenom-
enon may also occur among genotypes within tree species, and Madritch et al.
(2009) showed that coexisting clones of Populus tremuloides in forests in Wisconsin
caused distinct spatial mosaics of soil processes relevant to carbon and nitrogen
cycling. Finally, contrasting types of vegetation in the landscape can also differ in
their effects on the spatial heterogeneity of belowground properties. For example,
Kleb and Wilson (1997) found that woody vegetation promoted spatial hetero-
geneity of soil carbon and nitrogen relative to grassland vegetation, apparently due
to woody species producing a coarser root system. However, a recent synthesis of
global literature (Pärtel et al. 2008) showed that this pattern was apparent only in
temperate and not in tropical ecosystems.
Belowground biota are also affected by plants at a hierarchy of temporal scales
(Bardgett et al. 2005), due in a large part to temporal variability of resource input
to the soil (Wardle 2002). Different plant species and functional groups differ
greatly in the temporal variability of their resource production. For example, at a
regional spatial scale, Knapp and Smith (2001) found large differences in inter-
year variability of NPP across 11 sites in North America, with vegetation domin-
ated by herbaceous species showing greater variability than that dominated by
woody species. On a more local spatial scale, Wardle et al. (1999) found for a
72 • 3 Plant influences and plant–soil feedbacks

small plot experiment in a grazed grassland that different plant functional groups
differed in the temporal variability of their productivity, and that this in turn
affected the temporal variability of soil microbe and nematode densities. These
plant-driven effects on belowground temporal variability are likely to serve as
important temporal regulators of key ecosystem processes and the supply of plant-
available nutrients from soil.
Plant species within a community that provide resources in pulses are likely to exert
particularly important temporal effects on belowground organisms and processes
(Wardle 2002; Yang et al. 2008). For example, climatically driven pulsed phenomena
such as mast seeding can result in large quantities of reproductive material that decom-
poses and serves as a potential resource for decomposers. As such, Zackrisson et al.
(1999) showed that mast seeding in boreal forest by Picea abies provided a pulse of
readily available nitrogen that stimulated the growth of tree seedlings, presumably
through stimulating soil microbial activity, and similar effects may also result from
plant species that produce pulsed supplies of pollen (see Greenfield 1999). Further,
different coexisting plant species are also likely to differ greatly in relation to seasonal
production of resources; for example, deciduous tree species usually provide more distinct
pulses of litter fall than do evergreen species. In the shorter term, pulses of root exudates
are powerful drivers of root-associated microbes, and extrinsic factors that encourage
pulses of root exudates, such as foliar and root herbivory, in turn induce pulsed responses
of the soil biota (Bardgett and Wardle 2003; see also Chapter 4). However, despite
the likely importance of pulsed supply of plant-derived resources in an aboveground–
belowground context, this issue to date has been explored in comparatively few studies.

3.2.4 Multiple species effects

Plant species do not occur singly, but rather as members of multiple species commu-
nities. The issue that therefore arises is whether each species in that community exerts
effects on the belowground subsystem that are independent of those of the other
species. Since the mid-1990s this topic has been formulated as the so-called diversity-
function issue which seeks to address whether increasing plant species richness
influences ecological processes and properties (see review by Hooper et al. 2005),
but it nevertheless has a long historical basis. For example, agronomists have long
been interested in the potential benefits of multiple species cropping and intercrop-
ping (Vandermeer 1990), and Odum’s theory of ecosystem succession (Odum 1969)
speculated on whether species diversity altered the physical stability of ecosystems
and was a necessity for ‘long life of the ecosystem’.
The issue of how combinations of multiple plant species affect belowground organ-
isms and processes has been widely studied, and not just in recent years. For example,
Christie (1974, 1978) performed several conceptually simple experiments to show that
when pairs of plant species were grown together they could stimulate microbial
densities on each other’s roots relative to when they were grown separately (Fig. 3.5).
This means that mixtures of plant species could potentially stimulate microbial biomass
relative to corresponding plant monocultures. Further, in mixed stands of tree species,
 3.2 Plants and the belowground subsystem • 73

(a)
Bacterial cover Fungal mycelial length
7 4

Hyphal length (mm/mm2)

6
3
Bacterial cover (%)

4
2
3

2
1
1

0 0
Lolium Lolium Plantago Plantago Lolium Lolium Plantago Plantago
singly with singly with singly with singly with
Plantago Lolium Plantago Lolium

Litter respiration rate

(b)
50
Respiration (μg CO2-C g-1 h-1)

40

30

20

10

0
Spruce Oak Oak Pine Pine Alder Alder
with with with
spruce spruce spruce

Fig. 3.5 Early studies that provide evidence that plant species can have different effects on soil
biota and processes when grown in mixtures than when grown alone. (a) Cover by bacteria and
length of fungal mycelium on roots of each of two herbaceous plant species when grown in mixture
and grown singly. Lolium supports significantly more of both bacteria and fungi when grown with
Plantago than when grown alone (P < 0.025), while Plantago supports significantly more fungi
when grown with Lolium than when grown alone (P < 0.01). Derived from Christie et al. (1974).
(b) Litter-layer respiration rates in monocultures and two-species mixtures of different tree species.
Respiration in the spruceþpine mixture is greater than expected based on the component mono-
cultures while that for the spruceþalder and spruceþoak mixtures is less than expected (P < 0.001
in all cases). Derived from Chapman et al. (1988).
74 • 3 Plant influences and plant–soil feedbacks

Chapman et al. (1988) found that pairs of tree species grown together sometimes had
greatly different levels of litter respiration and densities of enchytraeids and earthworms
in the litter layer relative to when they were grown singly. This mixture effect could be
either positive or negative depending on the combination of tree species present
(Fig. 3.5). Other studies considering pairwise effects of plant species on soil processes
also show varied effects. For example, Wardle and Nicholson (1996) found that the
amount of soil microbial biomass present per unit root could either be promoted or
reduced by growing plant species in mixtures rather than monocultures, depending on
the plant species considered. Such studies point to pairwise combinations of plant
species strongly influencing the soil biota, albeit in varied directions.
Over the past 15 years many studies have been performed in which some measure of
the diversity of live plants (e.g. species richness, functional group richness, species
evenness) has been experimentally varied and various community or ecosystem re-
sponse variables subsequently measured (see Balvanera et al. 2006; Cardinale et al.
2006). Several of these have focused on the belowground subsystem, and the majority of
these find soil processes and/or densities of soil organisms to be either weakly affected or
unresponsive to the numbers of plant species or functional groups present (see Hooper
et al. 2005). A handful of studies do claim to present evidence for strong effects of plant
diversity on soil processes and biota, but such results appear to be specific for particular
experiments and approaches. This issue will be revisited in Chapter 5, but for the
purposes of this discussion it is apparent that while increasing plant species richness
from one to two or three species may exert either positive or negative effects on the
belowground subsystem depending on the species present, there is little consistent
evidence of a strong effect of increasing plant species richness beyond that.
One variant of the diversity manipulation approach that has been adopted in
many studies over the past two decades is the so-called litter-mixture approach.
Here, litters of two or more plant species are decomposed both singly and in
multiple species combinations, and the performance of each mixture is then
compared with what would be expected based on the average performance
of the litters decomposed singly. Litter-mixture studies have investigated the
effects of increasing diversity of litter types on a range of response variables,
including litter-mass loss rates, detritivore populations (Blair et al. 1990;
Hansen 2000) and community structure (Wardle et al. 2006; Ball et al. 2009),
nutrient dynamics (Ball et al. 2008; Meier and Bowman 2008), and temporal
variability of decomposer processes (Keith et al. 2008). The balance of evidence
points to mixtures of plant species having idiosyncratic effects on decomposer
processes and organisms, but with effects that are more often positive
than negative (see reviews by Gartner and Cardon 2004; Hättenschwiler
et al. 2005). While most studies have considered mixtures of two or three plant
species, those studies that have utilized mixtures of multiple plant species find
little evidence of increasing litter diversity beyond three species exerting
important ecological effects (e.g. Wardle et al. 1997a; Bardgett and Shine
1999; Perez Harguindeguy et al. 2008). Factors that regulate the effects of litter
mixing are discussed later in this chapter.
 3.3 Overriding effects of plant traits • 75

3.3 Overriding effects of plant traits

3.3.1 Contrasting plant species and trait axes
How plant species affect ecosystem properties is determined to a large extent by
their ecophysiological attributes or functional traits. It has long been recognized
that plant species (or groups of plant species) differ greatly in their traits, with traits
of species adapted for high resource availability differing from those of species
adapted for low resource availability (Grime 1977; Coley et al. 1985). For example,
conifers which are usually adapted for low-nutrient conditions characteristically
have low rates of tissue production, long-lived leaves, lower leaf nutrient concen-
trations, lower specific leaf areas, and lower maximum photosynthetic rates, com-
pared to angiosperm species (Cornelissen et al. 1996; Aerts and Chapin 2000).
Comparative studies involving multiple species also show consistent relationships
among these traits (e.g. Poorter and Remkes 1990), and provide evidence for an
axis of evolutionary specialization amongst species which reflects a trade-off
between the acquisition of resources and conservation of resources (Grime et al.
1997). Analysis of global data-sets containing plant trait (Díaz et al. 2004) or leaf
trait (Wright et al. 2004) data confirm the consistency of this trade-off across
contrasting floras and across major phylogenetic groups of vascular plants. As
such, Díaz et al. (2004) showed that the primary axis of specialization was
determined by traits relating to resource capture, usage, and release, with the
secondary axis being more related to traits reflecting plant size.
Plant trait combinations are important drivers of litter quality, and plant species that
are more adapted to nutrient-poor conditions and resource conservation generally
produce litter with lower concentrations of water soluble compounds, and higher
concentrations of structural carbohydrates such as cellulose and lignin and defense
compounds such as polyphenolics, than species adapted to high-resource conditions.
These properties of plant species adapted to poor resource availability make their leaf
litter less desirable for decomposer microbes and fauna; as a consequence, litter from
these species decomposes more slowly than species adapted to high-resource condi-
tions. As such, litter from coniferous species generally decomposes more slowly than
that from woody angiosperm species, which in turn breaks down more slowly than that
from herbaceous species (Enríquez et al. 1993; Cornelissen 1996). Comparative studies
of multiple plant species also shows litter mass loss to be related to a range of plant traits,
including plant growth rate (Cornelissen and Thompson 1997; Wardle et al. 1998a),
tissue strength (Cornelissen and Thompson 1997), and specific leaf area (Santiago 2007;
Kurokawa and Nakashizuka 2008). These studies collectively point to suites of leaf
traits as an important determinant of litter breakdown rates across species.
Recent studies have also focused on how plant traits might affect decomposability
of plant tissues other than leaves. For example, there is some evidence that root traits
may be correlated with leaf traits across species (Craine et al. 2002; Tjoelker et al.
2005; Freschet et al. 2010), suggesting that decomposability of root litter may be
driven by similar suites of traits that drive decomposition of aboveground litter
76 • 3 Plant influences and plant–soil feedbacks

(Wardle et al. 1998a). However, there is also evidence that plants may combine leaf
traits typical for fast-growing ‘competitor’ species with root traits typical for slower-
growing ‘stress tolerator’ species, or the other way round, and such reciprocal trait
combinations could potentially stabilize their co-existence (Personeni and Loiseau
2004). In forested ecosystems, tree species produce most of their biomass and litter as
wood. Little is understood about how decomposability of woody litter across plant
species is related to leaf traits, or how decomposability of wood litter is related to the
decomposability of leaf litter. However, a recent global meta-analysis (Weedon et al.
2009) revealed that gymnosperm wood litter decomposes more slowly than that from
angiosperms, and that wood traits such as concentrations of carbon and nitrogen and
the carbon-to-nitrogen ratio of wood were all related to wood decomposability, at least
for angiosperms. Further, there is recent evidence (Cornwell et al. 2009) that wood
traits determine not just the decomposability of wood, but also what proportion of it
enters the decomposer pathway as opposed to being consumed by fire or invertebrates.
While plant traits are well known to influence decomposition of plant litter, less is
known about the linkage between traits and soil organisms, or whether this has
multitrophic belowground consequences. Linkages between traits and belowground
biota are perhaps best understood for those soil organisms directly linked to plant
roots, notably mycorrhizal fungi. A synthesis of data for 83 British plant species
showed that mycorrhizal status is linked to plant traits such as relative growth rate
and foliar nutrient concentrations, as well as to the decomposability of leaf litter
(Cornelissen et al. 2001a) (Fig. 3.6). Specifically, ericoid mycorrhizae and to a lesser
extent ectomycorrhizae tend to be associated with plant species that have traits best
suited for acidic and resource-poor conditions, while arbuscular mycorrhizae are
associated with species that have traits more suited for base-rich and nitrogen-rich
but often phosphorus-poor conditions (Read 1991; Cornelissen et al. 2001a). Asso-
ciations of plant traits with soil organisms have been seldom explored explicitly for
the decomposer subsystem. However, Wardle et al. (1998a) found across 20 herb-
aceous plant species that the effect of plant species on microbial biomass (the primary
consumer trophic level of the soil food web) was significantly related to particular
root traits, such as specific root length, as well as some morphological aboveground
traits. This is suggestive of multitrophic consequences of plant traits. Across plant
species, consumption of dead leaves by litter-feeding invertebrates such as earth-
worms appears to be related to key traits such as leaf nutrient content (Hendriksen
1990). It has also been proposed that plant species which have traits associated with
more fertile environments are more likely to support bacterial-based rather than
fungal-based soil food webs (see Chapter 2), and to promote domination of the soil
meso- and macrofauna by earthworms and enchytraeids rather than by microarthro-
pods (Wardle et al. 2004a). Although there is evidence across habitats that this is
likely to be the case, direct experimental evidence under controlled conditions, for
example from common garden experiments that link plant traits to the abundance,
activity, and composition of decomposer food webs, is scarce.
While plant traits have long been recognized as important ecosystem drivers, recent
studies have highlighted that coexisting species may vary tremendously in their traits,
 3.3 Overriding effects of plant traits • 77

0.25 35
Mean RGR (g g–1 d–1)

0.20 30

Foliar N (mg g–1)

25
0.15
20
0.10
15
0.05
10
0.00
5
Ericoid (6)

Ecto (12)

Ecto/AM (8)

Woody-AM (26)

Forb-AM (11)

Gram-AM (16)
0

AM (26)

Gram-AM
Ericoid (6)

Ecto (12)

Ecto/AM

Forb-AM
Woody-

(11)

(16)
(8)
3.5 80
3.0
% Litter mass loss
Foliar P (mg g–1)

2.5 60
2.0
40
1.5
1.0
20
0.5
0.0 0
Ericoid (6)

Ecto (11)

Ecto/AM (8)

Woody-AM (26)

Forb-AM (11)

Gram-AM (16)

Ericoid (6)

Ecto (12)

Ecto/AM (8)

Woody-AM (26)

Forb-AM (11)

Gram-AM (16)

Fig. 3.6 Mean values (þ1 SE) for plant traits of six plant functional groups based on
mycorrhizal association type and life form. Numbers in parentheses refer to the number of
species. AM, arbuscular mycorrhizal fungi; RGR, relative growth rate in a standard growth-
chamber environment; Gram, graminoid. Mass-loss data are for a 20 week simultaneous
multispecies incubation in a litter bed. From Cornelissen et al. (2001a), with permission
from Springer ScienceþBusiness Media.

even over small spatial scales. For example, Hättenschwiler et al. (2008) showed that
45 coexisting Amazonian tree species varied three-fold in their litter nitrogen concen-
trations and seven-fold in their foliar phosphorus concentrations (Fig. 3.7). Further,
Richardson et al. (2008) collected foliar and litter samples from a 100 ha area of
temperate New Zealand rainforest representing a range of slopes and aspects, and
found over a 10-fold range in leaf nitrogen and phosphorus concentrations; this range
represented a large portion of the range reported globally for these nutrients (Fig. 3.7).
The ranges in leaf and litter nutrient concentrations found at local scales are likely to
have important knock-on effects to the decomposer subsystem. For instance, Cornwell
et al. (2008) synthesized data from 66 common garden decomposition experiments,
each involving a range of litter types decomposed in the same environment, and found
78 • 3 Plant influences and plant–soil feedbacks

(a)
0.6

0.5

0.4
Leaf P (%)

0.3

0.2 Global datasets

Ridge
Face
0.1 Gully
Terrace
0.0
0 1 2 3 4 5 6
Leaf N (%)
(b)

2.4
Litter P (⫻10) and N concentration (% DM)

2.0
N: factor 3

1.6

1.2

0.8
P: factor 7

0.4

0.0
44 46 48 50 52 54
Litter C concentration (% DM)

Fig. 3.7 Substantial variation in leaf and litter nitrogen and phosphorus concentrations over
relatively small spatial scales. (a) Range of leaf nitrogen and phosphorus concentrations for four
different landforms in a 100 ha area of rainforest in New Zealand, relative to that for global-scale
data-sets. From Richardson et al. (2008), with permission from Wiley-Blackwell. (b) Litter
phosphorus (P; circles) and nitrogen (N; squares) in relation to carbon (C) concentration for 45
coexisting Amazonian rainforest tree species; each species is represented by a different point. The
phosphorus and nitrogen concentrations vary by factors of three and seven respectively. DM, dry
matter. From Hättenschwiler et al. (2008), with permission from Wiley-Blackwell.
 3.3 Overriding effects of plant traits • 79

that rates of litter decomposition among species varied more than 10-fold within
experiments when the middle 90% of species (i.e. between the 5th and 95th percent-
iles) were considered. This compared with a 5.5–5.9-fold variation in decomposition
of common substrates in different biomes of greatly contrasting climate (see Berg et al.
1993; Parton et al. 2007) and points to the considerable importance of interspecific
variation in plant traits (notably those that drive litter quality) relative to the direct
effects of climate as a driver of plant litter decomposition.
Most studies on the effects of plant traits on the belowground subsystem have
considered only higher plant species, and few have considered other plant groups
such as ferns and bryophytes despite their likely role in driving nutrient cycling
(e.g. DeLuca et al. 2002b; Turetsky 2003) and regeneration of dominant tree species
(e.g. Coomes et al. 2005; Nilsson and Wardle 2005) in many forested ecosystems
worldwide (Fig. 3.8). However, Amantangelo and Vitousek (2008) found polyploid
and non-polyploid ferns in Hawai’ian rainforest to differ both with each other and with
coexisting vascular plant species in their leaf-litter chemistry. Further, Wardle et al.
(2002) found that litter from ferns in New Zealand rainforests had higher concentrations
of lignin and fibre and lower rates of decomposition than coexisting angiosperm species,
and that lignin concentration was an important predictor of differences in decomposition
rate among fern species. With regard to mosses, Wardle et al. (2003b) found litter from
feather mosses in boreal forest to decompose much more slowly than that from any of
the coexisting vascular plant species. Similarly, Dorrepaal et al. (2005) and Lang et al.
(2009) found for the sub-Arctic tundra that litter decomposition for moss species
(notably Sphagnum spp.) generally decomposed more slowly than that for vascular
species. Lang et al. (2009) also found large differences among moss and liverwort taxa
in terms of both litter quality and decomposition rate. The available evidence suggest
that ferns and mosses may differ greatly in their traits from that of higher vascular plants,
and that this may have important ecosystem-level consequences whenever these plants
are abundant. A likely consequence is the accumulation in the ecosystem of slowly
decomposing fern and bryophyte litter relative to faster-decomposing litter provided by
angiosperm species, as is evident for instance in high-latitude peatlands.
The vast majority of studies on the ecological impact of plant traits have focused on
across-species variability and neglected within-species variability, often by using a single
data point for each species. However, foliar and litter traits, notably nutrient concentra-
tions, may also vary several-fold within species (Richardson et al. 2005, 2008), and large
differences exist for litter decomposition rates within species both across environmental
gradients (Crews et al. 1995; Wardle et al. 2009a) and among genotypes (Schweitzer
et al. 2004; also see earlier discussion). It also appears likely, therefore, that variation in
key traits within a given species can affect the decomposer subsystem in the same way as
does variation in traits amongst species (Schweitzer et al. 2004). As such, assignment of
single trait values on a per-species basis, such as is commonly done in large traits
databases, has obvious limitations especially for species that have considerable plasticity.
Much remains to be understood about the importance of within-species variability, and
the relative role of within- and across-species variability in key traits, as drivers of the
belowground subsystem and ecosystem properties.
80 • 3 Plant influences and plant–soil feedbacks

(a)

(b)

Fig. 3.8 Few studies have considered the role of plant traits in affecting the decomposer
subsystem for lower plant species, despite their important role in driving ecosystem processes in
many ecosystems, such as ferns (e.g. Blechnum discolor) in New Zealand rain forest (a) and feather
mosses (e.g. Hylocomium splendens) in boreal forest (b). However, litter from these components
often decomposes much more slowly than that from the higher plants with which they coexist, and
as such may have an important role in driving belowground organisms and processes. Images by
D. Wardle (a) and A. Lagerström (b).
 3.3 Overriding effects of plant traits • 81

3.3.2 Trait dominance, trait dissimilarity, and multiple species effects

Plant species in any community differ greatly in their contribution to total biomass or
NPP. The mass ratio hypothesis proposed by Grime (1998) predicts that in a multiple-
species community the relative effect of each species on ecosystem properties should
be proportional to its relative contribution to the total NPP of the ecosystem. As such,
it serves as a useful framework for predicting the ecosystem-level consequences of
plant traits on ecosystem processes at a community-level scale, because it suggests
that the effects of the functional traits of each species in a given community on
ecosystem properties should be related to its contribution to the total productivity or
biomass of that community.
Some recent studies have used variants of this approach to relate ecosystem
process rates to community-weighted plant trait values, both above- and below-
ground. The procedure is conceptually straightforward: key functional traits are
measured for each species in the community and these traits are then weighted for
each species in terms of its proportional contribution to total community biomass.
These weighted trait values are combined to provide a community-aggregated value
for each trait, and ecosystem processes can then be related to these community-
aggregated trait values at the whole-community level. For example, Vile et al. (2006)
found that intersite variation in ecosystem NPP in a post-agricultural succession in
France could be predicted by using community-weighted values of a key functional
trait, namely relative growth rate. Similarly, community-weighted trait values for
functional leaf traits, for example specific leaf area, leaf dry weight matter content,
and leaf nitrogen concentration, have been shown to serve as effective predictors of
total plot-level litter decomposition rate across plots of primarily herbaceous vegeta-
tion in France (Garnier et al. 2004), Sweden (Quested et al. 2007), and throughout
Europe and Israel (Fortunel et al. 2009) (Fig. 3.9). Such studies point to the tract-
ability of scaling up from traits of individual leaves to process rates at the whole-
ecosystem scale.
Despite its obvious intuitive appeal, there are also two types of situation in which
the mass ratio hypothesis and community-aggregated trait values may be unable to
reliably predict community and ecosystem processes. The first situation involves
plant species that have disproportionate effects on ecosystem processes relative to
their contribution to total community biomass. For example, Peltzer et al. (2009) used
plant removal experiments in a primary successional New Zealand floodplain to show
that low-biomass invasive species had disproportionately large effects on soil micro-
bial and nematode communities in relation to their contribution to total plant com-
munity biomass (Fig. 3.10). Similarly, Wardle and Zackrisson (2005) used removal
experiments on islands with boreal forest to show that dwarf shrubs, which represent
only a small proportion of the total plant biomass present, had much greater effects on
plant litter decomposition, soil nutrients, and microbial biomass than did the trees and
mosses. The second situation occurs when the dominant plant species (or those that
drive ecosystem processes) have strong interactive (non-additive) effects on the
ecosystem process in question. There are numerous examples of this phenomenon
82 • 3 Plant influences and plant–soil feedbacks

(a)
50

Litter lignin-to-nitrogen ratio

40

30

20

10

(b)

18
Litter decomposability (g/kg/day)

16
14
12
10
8
6
4
2
0
0 100 200 300 400 500 600
Community-weighted mean LDMC (mg/g)

Fig. 3.9 Relationship of (a) litter lignin-to-nitrogen ratio and (b) litter decomposability at the
whole-plot scale with a community-aggregated value of a key leaf trait; that is, leaf dry matter
content (LDMC). Each point represents a different plot, and different symbols represent different
locations throughout Europe and Israel. From Fortunel et al. (2009), with permission from the
Ecological Society of America.

from litter-mixing studies, in which plant litter decomposition in multiple-species litter

mixtures can differ greatly from what would be expected based on the decomposition
of the components considered singly (Gartner and Cardon 2004; Hättenschwiler
et al. 2005; Ball et al. 2008; but see Hoorens et al. 2003). In this light, when aggregate
trait values have been used to predict plant-litter decomposition rates at the commu-
nity level, a considerable proportion of the total variation remains unaccounted for
(see Fortunel et al. 2009; Fig. 3.9). In any case, the mass ratio hypothesis provides a
useful null model for predicting ecosystem processes in multiple-species ecosystems,
 3.3 Overriding effects of plant traits • 83

(a) (b) (c)

(d) (e) (f)

Fig. 3.10 Differences in plant community structure at the time of harvest after 4 years of
plant-removal (exclusion) treatments applied to a primary floodplain succession in the
eastern South Island of New Zealand: (a) all species present (i.e. no plants excluded);
(b) both dominant shrub species (the native nitrogen fixer Coriaria arborea and the invasive
Buddleja davidii) present but all other non-native species excluded; (c) Buddleja excluded;
(d) Coriaria excluded; (e) Buddleja and Coriaria excluded; and (f) Buddleja, Coriaria, and
all other non-natives excluded. The experiment showed that Coriaria and Buddleja together
comprised 97% of aboveground biomass at the end of the experiment whereas other non-
native species comprised 3%; despite this the other non-natives had greater effects on soil
nutrients and belowground biota than did the two dominant shrub species, in contrast to the
predictions of the mass ratio hypothesis. From Peltzer et al. (2009), with permission from
Wiley-Blackwell.
84 • 3 Plant influences and plant–soil feedbacks

and exploration of situations in which it does not hold may yield useful insights
about the non-additive nature of multiple species effects in driving ecosystem
processes.

3.3.3 Ecosystem stoichiometery

One set of plant traits that has attracted considerable recent attention involves the
stoichiometric ratios of major elements, notably carbon, nitrogen, and phosphorus
(Koerselman and Meuleman 1996; Elser et al. 2000; Güsewell et al. 2003). At the
global scale, there is some evidence that leaf nitrogen-to-phosphorus ratios of forest
plants decrease with increasing latitude, indicative of increasing limitation by nitro-
gen relative to phosphorus (McGroddy et al. 2004). However, there is also consid-
erable variability in nitrogen-to-phosphorus ratios within biomes, as a result of
environmental variation in soil fertility, topography, and geology (Güsewell et al.
2003; Parfitt et al. 2005). For example, Townsend et al. (2007) found a 12-fold
range in the nitrogen-to-phosphorus ratio of rainforest trees in Costa Rica and
Brazil. Similarly, Högberg (1992) provided data showing large differences in foliar
nitrogen-to-phosphorus ratios for three functional groups of trees in savanna in
Zambia and Tanzania, with nitrogen-fixing arbuscular mycorrhizal species having
higher ratios than other arbuscular mycorrhizal species, and with both groups having
higher ratios than ectomycorrhizal species. Important differences even exist among
coexisting plant species; for example, Hättenschwiler et al. (2008) found foliar ratios
of carbon to nitrogen, carbon to phosphorus, and nitrogen to phosphorus to all vary
more than three-fold among 45 coexisting tree species in Amazonia. Similarly, large
differences were found in the nitrogen-to-phosphorus ratio among coexisting species
as well as within species (as a result of fertilizer treatments) in the mountains of the
north-west Caucasus in Russia (Soudzilovskaia et al. 2007).
The belowground subsystem is, however, only indirectly influenced by foliar
nutrient characteristics and more directly governed by litter nutrient properties.
Therefore, the amount of nitrogen and phosphorus resorbed by the plant from foliage
prior to litter fall is also an important determinant of the nutrient ratios of the
resources entering the decomposer subsystem. As such, litter often contains much
lower concentrations of nitrogen and phosphorus than does foliage from the same
species (Killingbeck 1996; McGroddy et al. 2004). The resorption potential by plants
of nitrogen and phosphorus, expressed in terms of concentration or pool sizes in
foliage relative to that of litter (Killingbeck 1996), also shows a several-fold difference
across environmental gradients both among and within species (Kobe et al. 2005;
Richardson et al. 2005), as well as among coexisting plant species (Hättenschwiler
et al. 2008; Wardle et al. 2009b). As such, and from a stoichiometric perspective, the
decomposer subsystem should be influenced by the combined effects of two sets of
live plant traits, i.e. the nutrient ratios of the leaves themselves, and the plant’s
resorption proficiency of these nutrients prior to litter fall.
There are several ways by which stoichiometric ratios of plant litter may in turn
impact on the decomposer subsystem. First, they can potentially affect elemental
 3.4 Plant–soil feedbacks • 85

ratios in tissues of decomposer organisms. A global literature synthesis by Cleveland

and Liptzin (2007) showed that ratios of carbon to nitrogen to phosphorus in the soil
microbial biomass were relatively constrained, even across large spatial scales and
types of ecosystems. However, some variation was present, which reflected the ratios
of these elements in the soil, and presumably in the litter input from the dominant
plant species. Further, Martinson et al. (2008) synthesized the limited amount of data
available on nutrient ratios for decomposer arthropods and found that there was some
variation in ratios of these elements across orders. Second, these ratios in turn affect
the activity of decomposer organisms, in terms of production of enzymes by the
decomposers (Sinsabaugh et al. 2008), and the enzymatic release of carbon and
nutrients from plant litter during decomposition. The regulation of litter decompos-
ition and nitrogen release by litter carbon-to-nitrogen ratios has been long recognized
(Swift et al. 1979), and there is increasing evidence that decomposer-driven processes
can be regulated by the availability of both nitrogen and phosphorus (Hobbie and
Vitousek 2000; Kaspari et al. 2008) as well as by the ratio of nitrogen to phosphorus
in litter (Wardle et al. 2002; Zhou et al. 2008). Therefore, as decomposition proceeds,
ratios of carbon to nitrogen to phosphorus of litter converge to values closer to that of
decomposer organism tissues. Third, the relative availability of carbon, nitrogen, and
phosphorus in the soil and in plant litter can serve as a powerful driver of the
decomposer microbe and invertebrate abundance and community structure (Wardle
et al. 2004b; Doblas-Miranda et al. 2008), the relative densities of bacteria and fungi
(Güsewell and Gessner 2009), and the body size distribution of soil animals (Mulder
and Elser 2009). These effects on decomposer organisms are in turn likely to have
important consequences for the processes of carbon and nutrient cycling that they
drive, and ultimately the functioning of the ecosystem.

3.4 Plant–soil feedbacks

It is apparent from the material presented so far in this chapter and in Chapter 2 that
plant species can select for particular soil communities and processes, and that soil
communities are in turn important drivers of plant growth and community compos-
ition. The consequence of this is that important feedbacks can exist between plant and
soil communities, in which individual plant species select for soil communities which
can then alter the success of both that plant species and of coexisting plant species
(Fig. 3.11). Many studies have explicitly studied this type of feedback, especially
over the past 15 years (e.g. Bever 1994; Van der Putten et al. 1993; Klironomos 2002;
Bezemer et al. 2006; Kardol et al. 2007). Although plant–soil feedbacks can be
inferred from a variety of approaches, a popular approach has involved the use of
‘feedback’ experiments, of which there are several variants, but the basic approach
involves two steps. First, soil (or soil inoculum) is collected that has been cultivated
by monocultures of known plant species, and which therefore contains the soil
communities associated with those species. Second, each plant species is then
grown in soil that has been cultivated both by its own species and by other species.
86 • 3 Plant influences and plant–soil feedbacks

Nutrients
Nutrients benefit
Pathogens Pathogens Mutualists Mutualists competing
benefit
attack attack benefit benefit species Y
species X
species X competing species X competing
species Y species Y
Enhanced
nutrient mineralization

Promotion of Promotion of Promotion

(–) (+) (+) (–) (+) (–)
pathogens mutualists of decomposers

Plant species Plant species Plant species

X X X
(a) (b) (c)

Fig. 3.11 Depiction of mechanisms by which a hypothetical plant species X can exert either
positive (þ) or negative () feedbacks with the soil community that it promotes, depending on
whether the mechanism mainly affects species X directly or exerts a stronger effect on
hypothetical competing plant species Y. (a) Pathogens, (b) mutualists, (c) decomposers.

This allows determination of the response of any given plant species to its own soil
community relative to that associated with other species. A positive feedback for a given
species exists when it performs better in its own soil than in soil from the other species; a
negative feedback exists when it performs worse. A third step can subsequently be
applied to identify the mechanistic basis of the feedback, through the use of soil analyses,
and soil sterilization and inoculation experiments (Kulmatiski and Kardol 2008).
Feedbacks between plant and soil communities can involve both the direct and
indirect pathways identified in Fig. 2.1 (Wardle et al. 2004a). Soil organisms that
interact with plants via the direct pathway include both those that have mutualistic
and antagonistic associations with the plants. Plant mutualists such as symbiotic
nitrogen-fixing bacteria and mycorrhizal fungi usually demonstrate a positive feed-
back with their host plant species, and there is a vast literature on the benefits to plant
species from these associations, as discussed in Chapter 2. As such, many plant
species select for nitrogen-fixing bacteria that greatly enhance their success under
nitrogen-poor conditions. Examples include Lupinus spp. on newly formed surfaces
following volcanic activity on Mount St Helens (Morris and Wood 1989), Alnus spp.
on freshly deposited gravels on floodplains (Walker 1989), and Carmichaelia
odorata colonization on newly formed alluvial river terraces (Bellingham et al.
2001). Similarly, plant species selection for a compatible mycorrhizal fungal com-
munity in turn has very well-known benefits for the plant through increasing its
access to soil nutrients and thus improving its nutrition (Smith and Read 1997). The
positive effect of plant species on their mycorrhizal associates also exerts important
effects at the community level. For example, there is evidence that mycorrhizal fungi
often promotes coexistence of plants and plant species, apparently through reducing
the intensity of competition (Grime et al. 1987; Hartnett and Wilson 1999; but
see Connell and Lowman 1989). Similarly, several studies have suggested that
 3.4 Plant–soil feedbacks • 87

mycorrhizal hyphal links among coexisting plants can be important in assisting the
establishment of new seedlings into communities, although the evidence for this is
mixed (Perry et al. 1989; Kytöviita et al. 2003; Selosse et al. 2006). While positive
feedbacks between plants and their mycorrhizal associates are undoubtedly common,
negative feedbacks are also theoretically possible, especially when a plant species
favours mycorrhizal fungal associates which then benefit competing plant species
(Bever 2003), or in fertile habitats where some plant species might even be adversely
affected by mycorrhizal fungi (Francis and Read 1995).
Soil pathogens and root herbivores in contrast usually demonstrate negative feed-
backs with plants. This is very well known for agroecosystems, and crop rotations are
routinely performed to reduce accumulation of soil-borne pathogens under particular
crop species. As mentioned in Chapter 2, negative feedbacks involving pathogens
have also become increasingly studied in other types of ecosystems and shown to
have important consequences for plant growth in several studies (Kulmatiski et al.
2008). For example, in a classical study in Dutch fore dunes, Van der Putten et al.
(1993) used soil feedback experiments to show that accumulation of pathogenic
nematodes under the pioneer plant species Ammophila arenaria contributed to a
decline of that species and enhancement of coexisting plant species, thereby promot-
ing vegetation succession. Similarly, studies on Prunus serotina in North America
(Packer and Clay 2000, 2003; Reinhart et al. 2005) provide evidence for accumula-
tion of oomycete pathogens under mature Prunus trees that greatly enhance Prunus
seedling mortality and reduce seedling growth. Sterilization of soil from under the
trees almost entirely eliminates seedling mortality (Packer and Clay 2000). Several
other studies using soil feedback experiments in native ecosystems also provide
evidence for negative feedbacks which are likely to result in a large part from soil
pathogen accumulation (e.g. Bever 1994; Klironomos 2002; Kardol et al. 2006, 2007;
Van der Putten et al. 2007; Petermann et al. 2008). However, plant–soil feedbacks
involving root pathogens need not always be negative, and the possibility theoretic-
ally exists for plant species to benefit from promoting pathogens that reduce the
fitness of competing plant species (Bever 2003).
As discussed in Chapter 2, decomposer organisms interact with plants via the
indirect pathway (Fig. 2.1) whereby plants provide resources for the decomposers as
plant litter and rhizosphere materials, and the decomposers in turn release nutrients
from these materials for plant growth. The relationship between producers and
decomposers is frequently mutualistic and therefore leads to a positive feedback.
For example, as discussed earlier in this chapter, the quantity and quality of organic
materials that plants input to the soil is often a powerful determinant of the abundance
and activity of decomposer microflora and soil fauna. Further, several studies have
shown that the composition of the decomposer community and structure of the soil
food web in turn influences plant growth rates and tissue nutrient concentrations
(Chapter 2; Wardle 2002), potentially altering the quantity and quality of the
resources that the plant produces. For example, Setälä and Huhta (1991) found that
addition of soil fauna to microcosms planted with seedlings of Betula pendula caused
an increase in shoot nitrogen concentration of more than 2.3-fold; the improved
88 • 3 Plant influences and plant–soil feedbacks

quality of litter subsequently produced by these seedlings would likely to be in turn

beneficial for the soil fauna. While positive feedbacks of this type are likely to be
important whenever a particular plant species dominates the soil under it, negative
feedbacks are also possible, especially when the plant promotes belowground con-
ditions that then promote competing plant species. For example, in moist heath lands
in The Netherlands, the dwarf shrub Erica tetralix dominates during early succession
when nutrient availability is low, but promotes accumulation of organic matter and
faster net nitrogen mineralization rates, in turn encouraging replacement of E. tetralix
by the grass Molinia caerulea which has a higher potential growth rate (Berendse
1998). This, and the rapid rate of mineralization of nitrogen from the new litter
produced by M. caerulea, sets a feedback in motion that disadvantages E. tetralix and
encourages further growth of M. caerulea (Fig. 3.2).
With regard to the indirect pathway, an intriguing possibility is that plant commu-
nities or species may select for decomposer communities that preferentially mineral-
ize their own litter (Wardle 2002). Despite the tractability of studying this question, it
has attracted surprisingly little attention to date. At the across-ecosystem scale, Hunt
et al. (1988) collected litter from the dominant plant species of an alpine meadow, a
pine forest, and a prairie in Colorado and decomposed all three litters in all three
habitats. In all cases, litter decomposed faster than expected in its own habitat relative
to when placed in either of the other habitats, suggesting that the vegetation in each
habitat selects for decomposers that break down its own litter (Fig. 3.12). Conversely,
Wardle et al. (2003a) collected litter of dominant species from each of 30 islands in
northern Sweden that differed greatly in vegetation composition, and decomposed
each litter on its own island and on other islands; here, placing litter in its site of origin
had no effect on decomposition. At the within-ecosystem scale, Vivanco and Austin
(2008) collected litter from each of three Nothofagus species in Patagonia, Argentina,
and decomposed each litter under each of the three species. In all cases they found
that litter decomposed fastest when placed under its own species, suggesting a
capacity for even closely related coexisting tree species to select for decomposers
that preferentially break down their own litter (Fig. 3.12). Similarly, Strickland et al.
(2009) found in an incubation study that recalcitrant tree litter decomposed faster in
the presence of microbial communities from forest ecosystems than from herbaceous
ecosystems, and Ayres et al. (2009) found that litters of three dominant tree species of
high-elevation forest in Colorado, USA, decomposed faster when they were incu-
bated with their own soil biota. Conversely, Ayres et al. (2006) performed a similar
experiment involving three tree species in northern England and failed to find such an
effect. When a plant species or community of plants selects for a soil community that
preferentially breaks down its own litter, it may potentially derive a competitive
advantage through having preferential access to nutrients released from that litter.
However, explicit tests of this have yet to be performed.
As is apparent through Fig. 3.11 and the above discussion, there are several
mechanisms through which plant–soil feedbacks can occur, and these can be either
positive or negative. This leads to the question of what the net effect of plant–soil
feedbacks is on plant growth, and this issue remains poorly understood. In a recent
 3.4 Plant–soil feedbacks • 89

(a)

20
Mass loss (%/yr)

10

0
O E O E O E
Prairie Meadow Forest

(b)
0.4
Decomposition constant (year–1)

0.3

0.2

0.1
N. dombeyi N. nervosa N. obliqua
Litter species

Fig. 3.12 Evidence that plant communities and species can select for decomposer communities
that preferentially decompose their own litter. (a) Results of a litter reciprocal transplant experiment
in which litter was taken from the dominant plant species in a prairie, a meadow, and a pine forest,
with each litter then being decomposed in all three habitats. For each habitat, O is the decomposition
rate observed when litter collected from that habitat was decomposed in the same habitat, and E is
the expected decomposition rate for litter from that habitat based on its decomposition rate in the
other two habitats. Overall the O and E values differ at P ¼ 0.001. Based on analysis of data
presented by Hunt et al. (1988). (b) Litter mass loss (expressed as decomposition constant) of litter
of each of three Nothofagus species decomposed under its own species (black bars) and under the
other species (white bars). The overall effect of location on decomposition is significant at P ¼
0.001. From Vivanco and Austin (2008), with permission from Wiley-Blackwell.

meta-analysis of 45 published studies, Kulmatiski et al. (2008) showed that net

plant–soil feedback effects were more often negative than positive, and suggested
that the high abundance of negative feedbacks could have important consequences
for structuring plant communities. However, such analyses need to be treated with
90 • 3 Plant influences and plant–soil feedbacks

caution for variety of reasons. First, most plant–soil feedback studies have been
performed in glasshouse studies that may encourage short-term proliferation of plant
antagonists relative to those that promote plant growth, especially when compared with
field situations. For example, short-term glasshouse studies may be unable to provide
conditions conducive to rapid development of soil macrofaunal communities and
mycorrhizal networks that promote plant growth. Second, the vast majority of feedback
studies done to date have involved herbaceous early-successional plant species, and it is
likely that positive feedbacks involving decomposer biota would be more important in
later successional systems which have a well-developed litter layer and are dominated
by woody plants. The indirect pathway between plants and soil biota (Fig. 2.1) is likely
to be important in reinforcing positive feedbacks between plants and decomposer biota,
especially if plant species can select for biota that preferentially decompose their own
litter. Much remains unknown about the net direction of plant–soil feedback effects on
plant growth, but it is likely that positive feedbacks are far more important than
suggested by the current balance of feedback studies performed to date.
Despite recent interest in plant–soil feedback, much remains unknown about how
these feedbacks are in turn important in structuring plant communities in real
ecosystems. Plant–soil feedbacks involving soil-borne antagonists may result in
enhanced coexistence of plant species especially if they disadvantage the dominant
plant species (Bonanomi et al. 2005; Kardol et al. 2006; Petermann et al. 2008). For
example, accumulation of pathogens under Prunus serotina leads to loss of domin-
ance by that species (Packer and Clay 2000) and therefore potentially a greater
abundance of its competitors. Such a mechanism may promote plant diversity, as
well as accelerate plant succession (discussed later in this chapter) and encourage the
success of invasive plant species (discussed in Chapter 5). Conversely, feedbacks
involving soil-borne antagonists may reduce plant species coexistence when they
disproportionately disadvantage subordinate species (Van der Putten 2005). Simi-
larly, plant–soil feedbacks involving mutualists or decomposers that benefit plant
growth could conceivably reduce species coexistence when dominant species are
favoured, or increase coexistence when subordinate species are favoured (Van der
Putten 2005). Indeed, there is theoretical evidence that plant–soil feedbacks involving
decomposition and mineralization processes could maintain plant species coexistence
and diversity, especially if each plant species in the community regulates the supply
of nutrients from the soil in its immediate vicinity (Huston and De Angelis 1994).

3.5 Succession and disturbance

The influence of plant species on belowground biota and processes, and the role of
plant–soil feedbacks, is highly apparent from studies on vegetation succession. Here,
plant-species composition changes over time on either newly formed surfaces (pri-
mary succession) or following disturbance events (secondary succession). The extent
and rate of this change is determined in a large part by others, notably facilitation
(where one or several species improve conditions for the establishment of one or
 3.5 Succession and disturbance • 91

Disturbance
Disturbance
Ecological process rates

Recovery

Recovery
Enhanced
retrogression

Build-up Maximal Decline or

phase biomass phase retrogression phase

Increasing N Increasing P
limitation limitation

Fig. 3.13 The build-up and decline or retrogressive phases of succession. The solid curves
represent primary succession while the dashed curves represent secondary succession. Adapted
from Walker et al. (2001), with permission from Wiley-Blackwell.

more species), competitive, or interference interactions, and tolerance by species of

the effects of other species (see Connell and Slatyer 1977; Pickett et al. 1987; Walker
and del Moral 2003). These interactions and species-replacement patterns are often
driven by changes in soil resource availability which itself changes during succes-
sion. Succession and ecosystem development consists of the build-up phase during
which plant biomass accumulates, the maximal biomass phase, and (given sufficient
time) the retrogressive or decline phase (Walker et al. 2001) (Fig. 3.13). The build-up
phase is characterized by the increased availability of nutrients (often nitrogen) while
the decline phase is characterized by declining availability of nutrients, especially
phosphorus (Vitousek 2004; Wardle et al. 2004b).

3.5.1 The build-up phase of succession

Upon the formation of new surfaces during primary succession, there is colonization
by both plant and soil communities. Although soil communities can establish inde-
pendently of plants (Bardgett et al. 2007a; Nemergut et al. 2007; Schmidt et al. 2008),
they mainly develop in association with the plant community. This applies to soil
biotic components that interact with plants both via the direct and indirect pathways
(Fig. 2.1). With regard to the direct pathway, communities of colonizing plant species
often include those that form symbiotic associations with nitrogen-fixing bacteria, and
which are well known to contribute greatly to the accumulation of ecosystem nitrogen
during the build-up phase (Morris and Wood 1989; Bellingham et al. 2001). During
this phase the mycorrhizal fungal community also develops, with colonizing plant
species preferentially selecting for strains of fungi that are characteristic of pioneer
92 • 3 Plant influences and plant–soil feedbacks

communities (Ishida et al. 2008) and with different plant species favouring different
fungal species (Pueschel et al. 2008). Over time the character of the mycorrhizal
community changes, in that while during early succession a proportion of the colon-
izing plants are non-mycorrhizal, in mid-succession the dominant herbaceous plants
tend to have a facultative requirement for arbuscular mycorrhizal fungi, while later in
succession the tree and shrub species which dominate often have an obligate need for
ectomycorrhizae (Read 1994). With regard to the indirect pathway, during early
succession different colonizing plant species are frequently associated with different
microbial communities (Bardgett and Walker 2004). As succession proceeds and there
is a greater amount of plant-derived organic matter in the soil, there is corresponding
colonization of soil invertebrates and development of the soil food web (Wardle 2002;
Bardgett et al. 2005; Neutel et al. 2007). Such development and changes in compon-
ents of the soil food web during vegetation succession are well documented and
include shifts from bacterial-dominated to fungal-dominated food webs (Ohtonen
et al. 1999; Bardgett et al. 2007a), increasing abundance of detritivorous meso- and
macrofauna (Kaufmann 2001; Doblas-Miranda et al. 2008), and enhanced densities of
invertebrate taxa known to be K- rather than r-selected (Wasilweska 1994). These
shifts are also accompanied by increasing food-chain length and complexity of the soil
food web (Wardle 2002; Hodkinson et al. 2004; Neutel et al. 2007).
Concomitant with changes in belowground communities that occur during vegetation
succession are changes in the rates of ecosystem processes driven by the soil biota.
Build-up of nitrogen during the initial stages of succession often results in the microbial
community shifting from being nitrogen-limited to carbon-limited, resulting in a
reduced loss of carbon through respiration per unit amount of microbial biomass
(Insam and Haselwandter 1989). This contributes to the rapid accumulation of organic
matter during primary succession, and which can be especially apparent when plant
species capable of significant nitrogen fixation are dominating (Halvorson et al. 1991).
As nitrogen availability increases and soil food webs develop, there is frequently a
greater rate of decomposition of plant litter (e.g. Crews et al. 1995) and supply rates of
nutrients, notably nitrogen, from the soil (Chapin et al. 1994). These changes in soil
processes can be driven by shifts in plant community composition succession, especially
when early successional species have large differences in functional traits to species that
dominate later (Berendse 1998; Grime 2001). However, as succession continues and the
maximal biomass phase is approached, a greater proportion of the ecosystem’s available
nutrients become immobilized in biological tissues. This contributes to a decline in plant
litter quality, activities of soil organisms, and rates of mineralization and supply of
available nutrients from the soil (Brais et al. 1995; Hättenschwiler and Vitousek 2000;
DeLuca et al. 2002a). At this stage, nutrients are cycled more conservatively, and both
aboveground and belowground communities can be colimited by nitrogen and phos-
phorus (Vitousek 2004). The eventual consequence of this limitation by nutrients is
ecosystem retrogression, which is discussed in section 3.5.2.
Plant species and their functional attributes may also be important drivers of the
disturbance regime that the ecosystem is subjected to (McIntyre et al. 1999),
and disturbances during the build-up and maximal biomass phases of succession
 3.5 Succession and disturbance • 93

frequently reverses successional development (Fig. 3.13). Major disturbances have

important effects on both the quantity and quality of the resources input to the
belowground subsystem, and this can influence both the soil biota and the processes
that they drive. For example, the formation of canopy gaps, a common consequence
of forest disturbance, can alter (and often impair) soil microbial biomass levels and
rates of litter decomposition and nutrient mineralization, presumably through a
reduction of plant-derived inputs (Bauhus and Barthel 1995; Zhang and Zak 1998;
Sariyildiz 2008). Forest damage through storms, notably hurricanes, can potentially
have far-ranging effects on belowground processes and organisms, through causing
immediate inputs of tree green-fall and mortality of fine roots (Herbert et al. 1999)
and longer-term reductions in the quantity and quality of litter inputs during stand
recovery (Hunter and Forkner 1999; Lugo 2008). Further, fire is a major contributor
to ecosystem disturbance regimes worldwide, and can exert a multitude of effects on
belowground organisms and processes (reviewed by Certini 2005). The most obvious
and widespread of these effects is to impair soil biota through causing loss of organic
matter (and, in forests, the humus layer), leading to a loss of habitat and resources for
soil organisms (Certini 2005). However, positive effects can also arise, for example
through fire encouraging domination by plant species that produce litter of superior
quality for decomposers (Nilsson and Wardle 2005), and the production of charcoal
that can greatly promote both soil microbial growth (Zackrisson et al. 1996) and the
belowground processes that they drive (Wardle et al. 2008b).

3.5.2 Ecosystem retrogression

In the long-term absence of catastrophic disturbance, characteristically in the order of
millennia, a decline or retrogressive phase often occurs which is associated with a
distinct reduction of plant biomass (Crews et al. 1995; Richardson et al. 2004; Wardle
et al. 2004b). This decline is accompanied by reductions in NPP, and shifts in the
respiratory and photosynthetic characteristics of the dominant vegetation (Turnbull
et al. 2005; Whitehead et al. 2005). Ecosystem retrogression has been characterized
for several long-term chronosequences around the world, including those initiated by
volcanic activity in Hawai’i (Crews et al. 1995; Vitousek 2004), isostatic land uplift
from the ocean in New Zealand (Ward 1988; Coomes et al. 2005), retreat of glacial
ice in New Zealand (Walker and Syers 1976; Richardson et al. 2004), wildfire in
northern Sweden (Wardle et al. 1997b, 2003a), and aeolian sand movement in
Queensland, Australia (Thompson 1981; Walker et al. 2001) (Fig. 3.14). This decline
phase is linked to long-term reductions in the availability of nutrients, notably
phosphorus (Walker and Syers 1976; Vitousek 2004), although increased soil
wetness through reduced soil drainage in old-growth forest could also sometimes
contribute (Coomes et al. 2005). As such, it has been suggested that during retro-
gression, phosphorus becomes more limiting relative to nitrogen. This is because
phosphorus is non-renewable and eventually becomes depleted from the ecosystem
or bound in increasingly unavailable forms while nitrogen can be renewed
by biological nitrogen fixation (Wardle et al. 2004b). In this light, ecologically
94 • 3 Plant influences and plant–soil feedbacks

(a) (b)

(c) (d)

Fig. 3.14 Reduction in forest plant biomass resulting from nutrient limitation due to ecosystem
retrogression (see Wardle et al. 2004b). (a, b) Forest at the maximal biomass phase (a) and long-
term retrogressive phase (b) for the Waitutu chronosequence in southern New Zealand (Ward
1988), a sequence spanning 600 000 years following uplift of land from the ocean; (c, d) forest at
the maximal biomass phase (c) and long-term retrogressive phase (d) for the Cooloola sequence in
Queensland, Australia, a sequence spanning 600 000 years following the formation of sand dunes
through aeolian sand movement. Images (a, b) by D.A. Wardle and (c, d) by R.D. Bardgett.

significant rates of non-symbiotic biological nitrogen fixation have been found for
ecosystems undergoing retrogression (Lagerström et al. 2007; Menge and Hedin
2009; Gundale et al. 2010). Consistent with this, there is evidence of a consistent
increase in nitrogen-to-phosphorus ratios of forest humus (and often of litter and
foliage) when long-term chronosequences enter a retrogressive phase, with ratios
tending towards values that are indicative of ecosystem limitation by phosphorus
rather than nitrogen (Wardle et al. 2004b) (Fig. 3.15).
 3.5 Succession and disturbance • 95

Cooloola Arjeplog

60 40

40
20
20

0 0

Glacier Bay Hawai’i

40 30

20
Ratio

20
10

0 0

Franz Josef Waitutu

40 40

20 20

0 0
Increasing time

Fig. 3.15 Nitrogen-to-phosphorus ratios for humus substrate (or uppermost mineral soil substrate
in the case of Cooloola) of each of six widely contrasting long-term chronosequences that have
undergone ecosystem retrogression, in relation to increasing time since the catastrophic disturbance
that initiated the chronosequence (expressed as a rank scale). The chronosequences are: Cooloola,
Queensland, Australia (caused by aeolian formation of sand dunes; spans 600 000 years); Glacier
Bay, Alaska (caused by retreat of glacial ice; spans 14 000 years); Franz Josef, New Zealand
(caused by retreat of glacial ice; spans 120 000 years); Arjeplog island sequence, northern Sweden
(caused by time since last fire, spans 6000 years); Hawai’i island sequence (surfaces formed by
volcanic activity, spans 4 100 000 years); and Waitutu, southern New Zealand (surfaces formed by
uplift from the ocean, spans 600 000 years). The Redfield ratio (nitrogen:phosphorus ¼ 16), above
which phosphorus is believed to become limiting relative to nitrogen (Redfield 1958), is shown for
comparative purposes in each panel as a dashed line. From Wardle et al. (2004b), with permission
from the American Association for the Advancement of Science.
96 • 3 Plant influences and plant–soil feedbacks

The reduced availability of nutrients and plant productivity in ecosystems that have
undergone retrogression has knock-on consequences for the key components of the
soil food web. For example, Wardle et al. (2004b) found while comparing six long-
term chronosequences worldwide that retrogression had generally negative conse-
quences for the soil microbial biomass, and often caused the microbial community to
become increasingly fungal- (as opposed to bacterial-) dominated. This is consistent
with fungal-dominated communities being better adapted for nutrient-poor conditions
and maintaining nutrient cycles that are more conservative in retaining nutrients, as
discussed in Chapter 2. Studies on decomposer soil fauna also reveal evidence for
multitrophic consequences of ecosystem retrogression. For example, studies on both
the Franz Josef Glacier chronosequence (Doblas-Miranda et al. 2008) and the Waitutu
chronosequence (Williamson et al. 2005) of New Zealand found that all major trophic
groupings of nematodes declined during retrogression, but that the ratio of fungal-
feeding nematodes to bacterial-feeding nematodes increased. This further suggests
that the fungal-based, rather than the bacterial-based, component of the soil food web
is favoured during retrogression, consistent with recent studies pointing to increasing
phosphorus limitation favouring domination by fungi (Güsewell and Gessner 2009)
and their consumers (Mulder and Elser 2009). Furthermore, measurements of a range
of soil-dwelling macroinvertebrate groups across the Franz Josef sequence by Doblas-
Miranda et al. (2008) revealed that while different taxa dominated at different stages of
the sequence, all taxa showed strong declines during retrogression regardless of body
size or trophic position. It is therefore apparent that the strong declines in nutrient
availability that occur in the order of millennia as retrogression proceeds exert
pervasive and strong bottom-up controls of the entire soil food web.
Diminished nutrient availability and impaired decomposer activity during retro-
gression in turn leads to reduced rates of decomposer processes and release rates of
nutrients from the soil. For example, decomposition rates of standardized substrates
across chronosequences show reduced rates of decomposition when placed in sites
that have undergone retrogression (e.g. Crews et al. 1995; Wardle et al. 2003a).
Furthermore, the release of nutrients during litter decomposition and rates of nutrient
fluxes driven by decomposer organisms are both generally slowed down as the
retrogressive phase is approached (Hobbie and Vitousek 2000; Vitousek 2004;
Wardle et al. 2004b). Retardation of decomposer processes during retrogression is
further enforced by the response of the dominant plant species in the community to
retrogression. During retrogression, plants resorb a greater proportion of their nutri-
ents from their foliage prior to litter fall (Richardson et al. 2005) and the quality of
litter entering the decomposer subsystem is therefore poorer (Crews et al. 1995;
Wardle et al. 2009a). This litter quality reduction occurs both across species
(i.e. species that dominate in retrogressive stages produce poorer-quality litter) and
within species (i.e. species that dominate across multiple chronosequence stages
produce poorer-quality litter during retrogression) (Richardson et al. 2005; Wardle
et al. 2009a). As such, reciprocal litter-transplant experiments, in which litters from
both non-retrogressive and retrogressive chronosequence sites are each decomposed
in both types of site, show that decomposer processes are impaired by retrogressive
 3.5 Succession and disturbance • 97

stands both through supporting a less-active microbial community and through

dominant species producing a lower quality of litter (Crews et al. 1995; Wardle
et al. 2003a). Impairment of decomposer processes and litter quality during retro-
gression may be partly reversible by fertilization of the nutrient that is most limiting
during retrogression; that is, phosphorus (Hobbie and Vitousek 2000).

3.5.3 Succession and plant–soil feedbacks

The plant–soil feedback mechanisms described earlier in this chapter (Fig. 3.11) can
serve as powerful determinants of species replacement and therefore vegetation
succession. Both positive and negative feedbacks can either maintain a given species
and thus retard succession, or encourage succession by encouraging replacement of a
given species by new species. Feedbacks during succession involve both the direct
and indirect pathways (Fig. 2.1), although the direct pathway has been by far the most
frequently studied.
Plant mutualists that exert a positive feedback with their host plant species are well
known as important drivers of succession. For example, many early successional
plant species form mutualistic associations with symbiotic nitrogen-fixing bacteria,
and while in the short term this benefits the host plant, in the longer term this leads to
improved soil nitrogen availability and therefore facilitation of later successional
plant species that then dominate. This is well known to contribute to species replace-
ment, with the earlier successional species being suppressed and excluded (Chapin
et al. 1994; Fastie 1995; Bellingham et al. 2001). Mutualisms between plant species
and mycorrhizal fungi may either enhance or retard succession. On one hand, pioneer
plant species may promote build-up of fungal species that can then serve as mutual-
ists with other later-successional plant species, leading to facilitation of these new
species and ultimately species replacement (Nara and Hogetsu 2004; Nara 2006). On
the other hand, mycorrhizal networks hosted by dominant plant species can also
encourage recruitment of seedlings of the same species (Dickie et al. 2002; Teste and
Simard 2008), potentially allowing that species to maintain dominance and thus
impair species replacement.
There is increasing recognition that negative plant–soil feedbacks can encourage
successional replacement of plant species, and several studies have tested this using
the feedback experimental approach described earlier in this chapter. Such studies
often find a given plant species to promote its soil-borne pathogens, leading to
accelerated succession by later successional species that are less susceptible to the
pathogens (Van der Putten et al. 1993; Kulmatiski et al. 2008). For example, Kardol
et al. (2006) used a feedback experiment involving plant species that dominate at
different stages of grassland succession to show that early-successional plant species
showed a negative plant–soil feedback while mid-successional species showed a
neutral feedback and late-successional species showed a positive feedback
(Fig. 3.16). This is indicative of a capability of earlier successional species to
influence the soil biota in such a way as to hasten successional replacement of
species. Further, De Deyn et al. (2003) used an experimental approach to show that
98 • 3 Plant influences and plant–soil feedbacks

Early-successional Mid-successional Late-successional

plants plants plants
200
Magnitude of plant–soil feedback

150

100

50

–50

–100
Early Mid Late Early Mid Late Early Mid Late
Soil origin Soil origin Soil origin

Fig. 3.16 Results of a soil feedback experiment in which 12 grassland plant species (four
species characteristic of each of early, middle, and late successional stages) were all grown in
sterilized soils collected from early-, mid-, and late-successional fields (first growth period), the
vegetation then harvested, then the soil replanted again with the same 12 species (second
growth period). For each bar, the soil feedback effect is the percentage change in plant growth
at the second growth period relative to that for the first growth period. * indicates that feedback
effect is significantly different to 0 at P ¼ 0.05. Derived from Kardol et al. (2006).

soil faunal communities extracted from soils differing in successional stage consistently
selectively impaired early successional plant species, thus encouraging species char-
acteristic of later successional stages. They attributed these effects to root-feeding
parasitic nematodes in the soil, suggesting that soil-borne antagonists can be import-
ant in encouraging the replacement of early successional plant species. Most studies
of this type have involved grassland successions, and whether such mechanisms can
also speed up succession in other ecosystem types such as forests remains largely
unexplored.
Fewer studies have considered the role of feedbacks between plants and the
decomposer subsystem (i.e. the indirect pathway in Fig. 2.1) in influencing succes-
sion. This is despite the ubiquity of these feedbacks in terrestrial ecosystems, and
their likely importance in influencing plant species replacement through affecting the
availability of soil nutrients. These feedbacks are driven in the first instance by plant
litter. For example, the study by Berendse (1998) discussed earlier provides evidence
that the dwarf shrub Erica tetralix promotes organic-matter build-up and increased
rates of nitrogen mineralization; this encourages domination by the grass Molinia
caerulea that in turn replaces E. tetralix. Conversely, if later successional plant
species produce litter that impairs decomposer activity, this could conceivably
impair species replacement. For example, maintenance of Pinus muricata dominance
in nutrient-poor sites in California could in part result from the trees producing
polyphenol-rich litter that is unfavourable for decomposer biota (or at least for
those decomposers that rapidly mineralize litter nutrients), leading to reduced
 3.6 Indirect effects of global change • 99

mineralization of nitrogen in the litter and therefore the availability of nitrogen to

competing plant species (Northup et al. 1995). Despite the well-known importance of
plant–decomposer feedbacks in determining plant growth, the consequences of these
for plant succession remain little understood.

3.6 Indirect belowground effects of global change

via vegetation
The Earth and its ecosystems are undergoing substantial and increasing modification as a
result of human-induced global change (Millennium Ecosystem Assessment 2005). The
principal global change drivers, namely climate change (including atmospheric carbon
dioxide enrichment), increased anthropogenic inputs of nitrogen, invasion of exotic
species, and land-use change, all act simultaneously to greatly modify both the compos-
ition and functioning of terrestrial ecosystems. As discussed in Chapter 2, the response of
belowground communities and the processes and feedbacks that they drive to global
change phenomena operate via both direct and indirect mechanisms. Direct effects of
global change on soil biological communities and the processes that they drive were
discussed in Chapter 2, largely in the context of carbon dynamics and climate change.
Here, we consider how effects of global change phenomena on soil communities and the
ecosystem-level functions and feedbacks that they drive are affected indirectly by
changes in the productivity and shifts in composition of plant communities. Indeed, we
argue that an understanding of the effects of these global change phenomena on terrestrial
ecosystems, and also their potential mitigation for instance through soil carbon seques-
tration, requires explicit consideration of linkages between aboveground and below-
ground subsystems (Wolters et al. 2000; Wardle et al. 2004a; Tylianakis et al. 2008;
Bardgett et al. 2008; Kardol et al. 2010). We illustrate this using climate change and
nitrogen enrichment as examples, whereas effects of invasive species will be considered
in Chapter 5. We do not provide an exhaustive review of the indirect impacts of these
global change phenomena on soil biological properties and ecosystem-level feedbacks,
which is beyond the scope of this book; rather, we use selected examples to illustrate key
mechanisms at play.

3.6.1 Indirect belowground effects of climate change

Rising atmospheric concentrations of carbon dioxide represents the clearest and most
documented signal of human alteration of the Earth-system (IPCC 2007); since pre-
industrial years (pre-1800), atmospheric carbon dioxide concentrations have risen by
some 30% from 280 to 365 ppm, due mostly to the burning of fossil fuels and
clearance of natural lands for agriculture, and, depending on future trends, they
could reach 540–970 ppm by the end of this century. This rise in atmospheric carbon
dioxide has already substantially affected the world’s climate, and the consensus is
that it will force further change in coming years, leading to a rise in average
temperatures and a greater occurrence of extreme weather events (IPCC 2007).
100 • 3 Plant influences and plant–soil feedbacks

These changes in climate have the potential to have marked indirect effects on soil
biological communities and their activity, and therefore feedback to climate change,
by influencing plant growth and vegetation composition, and therefore the allocation
of carbon belowground. Such plant-mediated indirect effects of climate change on
belowground communities can operate via a variety of mechanisms, but can broadly
be separated into two (Bardgett et al. 2008; Kardol et al. 2010). First, rising atmos-
pheric concentrations of carbon dioxide can indirectly impact on soil microbes and
their predators via increased plant photosynthesis and transfer of photosynthate
carbon to fine roots and soil biota, and through altering plant litter quality. Second,
in the longer term indirect effects of climate change on soil organisms and their
activity operate via shifts in the functional composition and diversity of vegetation.
We now discuss these mechanisms in turn.
It is well established that elevated carbon dioxide increases plant photosynthesis
and growth, especially under nutrient-rich conditions (Curtis and Wang 1998; De
Graaff et al. 2006), and this in turn increases the flux of carbon to roots, their
symbionts, and heterotrophic microbes via root exudation of easily degradable
sugars, organic acids, and amino acids (Zak et al. 1993; Diaz et al. 1993; Iversen
et al. 2008). The consequences of increased carbon flux from roots to soil for
microbial communities and carbon exchange are difficult to predict, because these
effects are influenced by a range of factors including plant species identity and traits,
soil food web interactions, and soil fertility. However, we can identify some possible
outcomes for soil organisms and carbon exchange. For instance, increased below-
ground allocation of carbon to roots, and its transfer from roots to soil, can stimulate
microbial abundance and activity, enhancing the mineralization of both recent and
old soil organic carbon (i.e. priming), and hence carbon loss from soil (Körner
and Arnone 1992; Zak et al. 1993; Freeman et al. 2004; Heath et al. 2005; Fontaine
and Barot 2005; Kuzyakov 2006; Dijkstra and Cheng 2007; Jackson et al. 2009).
Indeed, several free-air carbon dioxide enrichment (FACE) experiments have shown
that elevated carbon dioxide can lead to substantial increases in root biomass and soil
respiration (e.g. Körner and Arnone 1992; Hungate et al. 1997; Norby et al. 2004;
Pritchard et al. 2008; Jackson et al. 2009), and that, in general, belowground
responses to elevated carbon dioxide are often greater than aboveground responses
in the same systems (Jackson et al. 2009). As highlighted in the previous chapter,
mycorrhizal fungi also act as a significant sink for recent plant photosynthate
(Högberg and Read 2006), and increased supply of photosynthate carbon to these
fungi under elevated carbon dioxide can stimulate their growth (Rillig et al. 2000),
especially under conditions of low nutrient availability (Klironomos et al. 1997;
Staddon et al. 2004). This can in turn feed back positively on plant growth and
hence carbon assimilation. Changes in the growth of mycorrhizal fungi in response to
elevated carbon dioxide concentrations can also potentially influence soil and eco-
system-level carbon dynamics by controlling the release of carbon to the soil micro-
bial community (Högberg and Read 2006), and by enhancing the stabilization of soil
organic carbon through promotion of soil aggregation (Rillig and Mummey 2006; Six
et al. 2006; De Deyn et al. 2008; Wilson et al. 2009).
 3.6 Indirect effects of global change • 101

Conversely, the stimulation of microbial biomass as a result of enhanced root

carbon supply can lead to immobilization of soil nitrogen, thereby limiting nitrogen
availability to plants (Diaz et al. 1993; De Graaff et al. 2007), creating a negative
feedback that constrains future increases in plant growth and carbon transfer to soil.
Also, increased plant-microbial competition for nitrogen, which as discussed in
Chapter 2 can lead to reduced soil nitrogen availability and microbial activity, can
suppress microbial decomposition, leading to increased ecosystem carbon accumu-
lation (Hu et al. 2001). A key mechanism here is likely to be reduced substrate
quality, in that elevated carbon dioxide concentrations reduce nitrogen concentrations
of plant tissue, resulting in larger carbon-to-nitrogen ratios of litter inputs entering
soil (Curtis and Wang 1998; Coûteaux et al. 1999). This in turn leads to nitrogen
limitation of the microbial biomass, resulting in nitrogen immobilization and a
reduction in the supply of nitrogen to plants, thereby constraining the fertilizing
effects of elevated carbon dioxide on plants (Curtis and Wang 1998; Coûteaux et al.
1999). Interestingly, a recent meta-analysis by De Graaff et al. (2006) of data from
117 studies revealed that on average elevated carbon dioxide stimulated gross
nitrogen immobilization and microbial nitrogen by 22 and 5.8% respectively, and
increased microbial biomass and soil respiration by 7.1 and 17.7%, respectively.
However, this meta-analysis revealed that elevated carbon dioxide stimulated overall
plant biomass substantially, especially when additional nitrogen was added, thereby
outweighing carbon loss through microbial respiration and causing a net increase in
soil carbon of 1.2% per year. Other studies have shown that in unfertilized ecosys-
tems microbial nitrogen immobilization enhances acclimation of plant growth to
elevated carbon dioxide in the long-term (Finzi et al. 2002; De Graaff et al. 2006).
As such, increased soil carbon input and sequestration under elevated carbon dioxide
can only be sustained in the long term when additional nutrients are supplied,
for instance from fertilizers or atmospheric nitrogen pollution (Finzi et al. 2002;
De Graaff et al. 2006). The decline in nitrogen availability under elevated carbon
dioxide is central to the progressive nitrogen limitation concept, whereby in the
absence of new nitrogen inputs (e.g. from fertilizers or nitrogen pollution) the
availability of nitrogen declines over time at elevated carbon dioxide relative to its
availability at ambient carbon dioxide levels (Luo et al. 2004).
In the longer term (decades to centuries), climate change indirectly influences the
belowground subsystem via shifts in the functional composition and diversity of
vegetation. It is well established that global warming and altered precipitation
regimes can alter the distribution of plant species and functional groups at both
local and global scales (Prentice et al. 1992; Woodward et al. 2004). For instance,
recent changes in precipitation patterns have markedly affected vegetation compos-
ition in tropical rainforest (Engelbrecht et al. 2007) and African savanna (Sankaran
et al. 2005), and warming is leading to rapid replacement of Canadian tundra by
boreal forest (Danby and Hik 2007), declines in cryptogam abundance (mosses and
lichens) (Cornelissen et al. 2001b; Walker et al. 2006), rapid losses of plant diversity
in salt marshes (Geden and Bertness 2009), pan-Arctic shrub encroachment in Arctic
tundra (Sturm et al. 2001; Epstein et al. 2004; Tape et al. 2006; Wookey et al. 2009),
102 • 3 Plant influences and plant–soil feedbacks

and widespread increases in tree mortality rates in the western USA (Van Mantgem
et al. 2009). Likewise, elevated atmospheric carbon dioxide has been shown to cause
shifts in the vegetation composition of grassland (Körner et al. 1997; Niklaus et al.
2001), in some cases promoting the growth of legumes with consequences for soil
nitrogen cycling (Newton et al. 1995; Hanley et al. 2004; Ross et al. 2004). Such
shifts in vegetation composition influence the uptake of carbon dioxide by photo-
synthesis (Reich et al. 2001; Ward et al. 2009) and hence the transfer of photo-
synthate to soil, and also modify the soil physical environment for example by
changes in root architecture and rooting depth (Jackson et al. 1996). However, the
main route by which climate-driven shifts in vegetation composition influence soil
organisms over longer timescales is via changes in the quality and quantity of organic
matter entering the soil as plant litter, which as discussed previously in this chapter
act as primary drivers of the biological properties of soil.
One well-documented example of the belowground consequences of shifts in
vegetation composition resulting from global warming comes from the Arctic
(reviewed by Wookey et al. 2009) (Fig. 3.17). It is well known that high-latitude
and alpine ecosystems will be especially responsive to rapid climatic warming in
coming decades (Overpeck et al. 1997; Serreze et al. 2000; Euskirchen et al. 2006),
and a consequence of this is the expansion of dwarf-shrubs, such as Betula nana
(Hobbie et al. 1999; Sturm et al. 2001; Epstein et al. 2004; Jónsdóttir et al. 2005; Tape
et al. 2006). Dwarf-shrubs produce leaf litter and woody material of much poorer
quality, and hence lower decomposability, than the graminoids and forbs that they
replace (Cornelissen 1996; Quested et al. 2003; Dorrepaal et al. 2005). The conse-
quences of this for carbon-cycle feedbacks in the Arctic are uncertain, but it was
recently suggested by Cornelissen et al. (2007) that warming-induced expansion of
shrubs with recalcitrant leaf litter across cold biomes would constitute a negative
feedback to global warming, potentially countering the direct warming enhancement
of decomposition and hence carbon loss from Arctic soils. This conclusion was based
on the results of a large-scale quantitative analysis of the major climate-change-related
drivers of litter decomposition rates in cold northern biomes worldwide, which
showed that both plant growth form and direct climate effects were the principal
drivers of litter decomposition rate (Fig. 3.18). Specifically, Cornelissen et al. (2007)
found that litter of the predominant plant species in 33 experiments in Arctic and
alpine sites in the Northern Hemisphere decomposed on average 42% faster in warmer
than colder soils (representing 3.78C higher soil temperatures sustained over a longer
growing season), and on average grass and sedge litters were decomposed 40% faster
than shrub litter (Fig. 3.19). Interestingly, these finding are consistent with those of the
previously mentioned study of Cornwell et al. (2008) who analysed mass-loss data for
818 plant species from 66 decomposition experiments on six continents and found that
the magnitude of species-driven differences in decomposition are much larger than
previously thought and greater than climate-driven variation.
In drawing conclusions on how increased shrub expansion will affect large-scale
soil carbon stocks in the Arctic, other feedbacks on the carbon cycle resulting
from climate warming and increasing shrub encroachment need to be considered
 3.6 Indirect effects of global change • 103

SPECIES EFFECTS EMERGENT PROPERTIES

Biotic drivers of
encroaching species Susceptibility to fire
Predators Canopy and soil
microclimate
Energy budget
HERBIVORES GROWTH
AND
ALLOCATION
Carbon balance

COMPOSITION OF LITTER
PLANT FUNCTIONAL TYPES DECOMPOSITION

Trace gases

UPTAKE
Hydrology
Free-living
soil fauna
External biotic drivers

Fig. 3.17 Conceptual framework for considering the internal linkages and feedbacks associated
with a shift in plant functional types (PFTs) on ecosystem-level properties in the Arctic, from
Wookey et al. (2009). Changes in PFTs (left-hand box, Species Effects) will feed forward to affect
consumers (both herbivores and decomposers) through changes in the quality, quantity, and timing
of food availability, as well as changing habitat physical characteristics, for example shelter for
small herbivores (e.g. invertebrates, small rodents, and birds). Where feedbacks occur between two
components of the ecosystem they are indicated by bidirectional arrows. In the decomposition
subsystem feedbacks are exerted through potential shifts in the magnitude, timing, and location
(e.g. in the rhizosphere versus at the soil surface or the interface of dead roots) of nutrient
mineralization, alterations in mycorrhizal associations, and competition between decomposers
and autotrophs for nutrients. Changes in the composition of PFTs, and in plant growth and
allocation patterns, interface directly with the Earth-system by influencing ecological properties
and processes that affect energy and water exchange, soil fertility and physical structure, or
susceptibility to fire, while whole-ecosystem metabolism across trophic levels affects carbon fluxes
(both gaseous and aqueous). From Wookey et al. (2009), with permission from Wiley-Blackwell.

(Cornelissen et al. 2007). First, it is unclear how the negative effect of shrub expansion
on decomposition compares in magnitude with changes in decomposition driven by
changes in snow cover, which could be either positive or negative (Chapin et al. 2005;
Sturm et al. 2005; Weintraub and Schimel 2005; Wookey et al. 2009). Second, because
shrubs tend to have shallower root systems than do graminoids, decomposition of their
root litter might be enhanced by warming of upper soil horizons, thereby enhancing soil
carbon loss (Mack et al. 2004). Third, the build-up of litter resulting from increased
productivity and associated litter production of shrubs (Shaver et al. 2001), combined
 Equator

104 • 3 Plant influences and plant–soil feedbacks

10° P < 0.001,
20° Litter Incubation Life Zone (LILZ)
30° df = 1
40° Growth Form (GF) P< 0.001, df = 5

50° Site of Litter Origin (SLO) P< 0.001, df = 32

9
60° SLO * GF P< 0.001, df = 36

7 8 70° GF * LILZ P< 0.001, df = 5

6
Global Change Treatment (GCT) P= 0.003, df = 9
80° 10
90°W North Pole 90°E SLO * GCT P< 0.001, df = 54

GF * GCT P = 0.134, df = 29
1
2 SLO * LILZ P= 0.024, df = 32
18
4
13–17 GCT * LILZ P = 0.218, df = 9
3 12 5
0 50 100 150 200 250
11 Explained variance/residual variance

33 Arctic and Alpine Field Experiments in the Meeting of Litters:

1. Ny Ålesund, Svalbard, Norway (F,I) 7. Ruby Range, Canada (W,F) 13. Latnjajaure, Sweden (3 exp.; W,F)
2. Adventdalen, Svalbard (2 exp.; UV,W) 8. Toolik Lake, Alaska, USA (W,F,SH) 14. Abisko, Sweden (4 exp.; W,F,I,CO2,UV)
3. Thingvellir, Iceland (W) 9. Tateyarna, Japan (W) 15. Paddus, Sweden (2 exp.; W,F,SH)
4. Audkuluheidi, Iceland (W) 10. Qinghai, China (4 exp., W) 16. Slåttatjåkka (Abisko), Sweden (W,F,SH)
5. Caucasus, Russia (F,I) 11. M. Rondinaio, Italy (2 exp., F) 17. Stordalen, Sweden (2 exp.; W,CO2,F)
6. Medicine Bow, USA (2 exp.; W) 12. Finse, Norway (2 exp.; W,F) 18. Kilpisjärvi, Finland (2 exp.; W,F)

Treatments: W, warming; F, fertilising; I, irrigation; CO2, elevated CO2 concentration;

UV, elevated UVB irradiance; SH, shading

Fig. 3.18 Analysis of the key biotic and abiotic drivers of percentage mass loss of leaf litters (right), based on decomposition of litter collected from
the predominant plant species in 33 global change-mimicking experiments in Arctic and alpine sites in the Northern Hemisphere. All leaf litters were
incubated in a common litter bed at two contrasting litter incubation life zones (LILZs). One LILZ was at high altitude and the other was at low
altitude: the ‘meeting of litters’ experiment (left). From Cornelissen et al. (2007), with permission from Wiley-Blackwell.
 3.6 Indirect effects of global change • 105

90 a Abisko (milder life zone)

80 Latnja (colder life zone)

Percentage litter mass loss

v b b
70
w
60
x c c c
50
y
40 z xyz
30
20
10
0

6)

7)
9)
7)
8)

7)
11

,5
,3
,3
,6

,
(7
5
1,
3
2
8

(6
(4
(4
(8

SS
(1

B
E
SS
B

O
U
B
G
R

M
A

R
U
FO

D
R

SH
R
SE
G

SH

N
EE
S
U

R
O

G
U

ER
ID
EC

EV
D

Fig. 3.19 Mean mass-loss data (%) of leaf litters from predominant plants of six growth forms
collected from ambient plots in circumarctic-alpine sites (Fig. 3.18), after 2 years of outdoor
incubation in two contrasting litter incubation life zones (LILZs). Numbers in parentheses refer
to replication in the milder LILZ (Abisko) and the colder LILZ (Latnjajaure), respectively.
ANOVA output: growth form (GF): F ¼ 84.7, P < 0.001; LILZ F ¼ 50.0, P < 0.001; GF by
LILZ interaction F ¼ 0.98, P ¼ 0.43. Standard errors are shown one-sided. Within each LILZ,
growth forms with the same letter are not significantly different in post-hoc Games–Howell
tests. From Cornelissen et al. (2007), with permission from Wiley-Blackwell.

with their lower rates of decomposition, may increase fuel loads and the flammability of
the litter layer, thereby promoting fire-induced carbon loss to the atmosphere. The
magnitude of this increase, however, will depend on trends in precipitation and soil
hydrology (Chapin and Starfield 1997; Hobbie et al. 2001; Cornelissen et al. 2007).
Fourth, Arctic plant functional groups differ in their association with microbial com-
munities (Wallenstein et al. 2007; Wookey et al. 2009) and mycorrhizal status (Read
et al. 2004), so climate-driven shifts in vegetation composition might affect the capacity
of microbes to decompose plant litter. This could in turn alter nutrient competition
between plants and soil microbes with possible consequences for ecosystem nutrient
cycling and soil carbon exchange (Bardgett et al. 2008). Finally, as noted by Cornelissen
et al. (2007) the relative strengths of these various feedbacks due to growth form shifts
need to be considered in the context of longer-term warming effects on deep soil carbon
dynamics (Mack et al. 2004) and of positive feedbacks on carbon cycling from
disturbances such as land use and herbivory (Wookey et al. 2009).
The above example from the Arctic provides evidence of the strong effect of
interactions between plant traits and the belowground subsystem on ecosystem
106 • 3 Plant influences and plant–soil feedbacks

carbon stocks under climate change. As recently reviewed by De Deyn et al. (2008),
there is now a growing body of literature showing that soil carbon pools of terrestrial
biomass across the globe can be related, in part, to key plant traits and their links with
soil biota (Fig. 3.20). These linkages, which operate via a variety of mechanisms at
different spatial and temporal scales, govern the assimilation of carbon, its transfer to
soil and residence time, and its loss from soil via decomposition processes (Fig. 3.21).
While our understanding of the mechanisms by which plant traits influence soil
carbon storage is incomplete, these authors argued the need for a mechanistic
approach to soil carbon sequestration which implicitly includes the traits of soil
biota through their link with plant traits. Importantly, such a trait-based approach
could help in the development of strategies to promote carbon sequestration, thereby
mitigating increasing atmospheric carbon dioxide concentrations (Lal 2004; P. Smith
et al. 2008; Díaz et al. 2009). However, empirical studies are needed to identify
general mechanisms by which plant traits and their combinations alter the amount and
quality of plant inputs to the soil, and how this can be incorporated into management
regimes to promote ecosystem services such as carbon storage (Wardle et al. 2003a;
Fornara and Tilman 2008; De Deyn et al. 2008, 2009; Steinbeiss et al. 2008; Jonsson
and Wardle 2010).

5000

4000

19.1
MAP (mm year–1)

3000 Tropical forest

Aboveground
productivity,
7.1 fast cycling,
AM, N-fixers,
2000 Temperate forest soil engineers
C-cycling traits: soil fertility and
9.4
19.3 herbivory dependent, EM, AM,
Boreal forest soil engineers
5.4
1000 Frost, anoxia, slow 12.7 Savanna
cycling, E(C)M, fire Grassland 13.3
21.8 Drought, grazing, fire,
C-cycling traits: soil fertility and
Frost, anoxia
herbivory dependent; AM, N-fixers, engineers AM, N-fixers, engineers
Tundra slow, E(C)M
9.9 Desert Drought tolerance, slow cycling, abiotic mineralisation 1.4
0
–15 –5 5 15 25
MAT (°C)

Fig. 3.20 Soil organic carbon pools (kg C m2; Amundson 2001), and drivers of plant carbon
sequestration traits across biomes with characteristic mean annual temperature and precipita-
tion (MAT and MAP). Lower and higher values within biomes represent warm versus cool-
temperate forest, respectively, and drier versus wet (peaty) tropical forests; EM, ecto-; ECM,
ericoid-; AM, arbuscular mycorrhizal fungi; biome location after Woodward et al. (2004).
Adapted from De Deyn et al. (2008), with permission from Wiley-Blackwell.
 3.6 Indirect effects of global change • 107

Soil fertility

Primary Plant species Plant trait

productivity competition composition

Complementing Mutualism
resource use traits
Soil abiotic conditions:
moisture, temperature, pH
Litter traits
Soil aggregate formation:
Litter Rooting profile
Litter quality soil biota activity
quantity + –

Enhanced Reduced
decomposition decomposition
Soil
structuring
Herbivory Fire Fire C, N, P
immobilization
CO2,CH4
C, N, P Recalcitrant SOC
mineralization metabolites stabilization
C-out C-in
Trait composition enhances soil carbon sequestration when DC-out< DC-in

Fig. 3.21 Potential effects of plant trait composition on soil carbon sequestration, as mani-
fested through influencing the ratio between carbon gains and losses. SOC, soil organic carbon.
Adapted from De Deyn et al. (2008), with permission from Wiley-Blackwell.

3.6.2 Indirect belowground effects of nitrogen deposition

Human activities have lead to major increases in global emissions of nitrogen to the
atmosphere, causing dramatic increases in deposition of atmospheric nitrogen to the
terrestrial biosphere (Holland et al. 1999; Bobbink and Lamers 2002; Galloway et al.
2004). As with climate change, nitrogen enrichment also has the potential to signifi-
cantly affect the belowground subsystem and ecosystem-level processes via vegeta-
tion change. Because most plant communities are limited by nitrogen (Vitousek and
Howarth 1991), the addition of nitrogen substantially alters their productivity and
structure, typically favouring fast-growing species that are able to exploit this re-
source, enhancing NPP. For instance, studies in alpine tundra indicate that nitrogen
enrichment causes a shift in community composition in favour of graminoids and
sedges over forbs (Bowman et al. 1993, 1995; Soudzilovskaia et al. 2007) and
bryophytes (Van der Wal et al. 2003). Similarly, studies of temperate grasslands
show that nitrogen enrichment enhances the growth of grasses at the expense of
legumes and forbs (Bobbink 1991; Wedin and Tilman 1996; P. Smith et al. 2008),
whereas in Arctic tundra increases in woody deciduous shrubs such as Betula nana
(Bret-Harte et al. 2002; Hobbie et al. 2005) and graminoids (Press et al. 1998; Shaver
et al. 1998; Gough et al. 2002) commonly occur.
108 • 3 Plant influences and plant–soil feedbacks

Nitrogen enrichment increases the amount and quality of litter entering soil, both
through promoting the dominance of faster-growing plant species, and through
enhancing leaf nitrogen concentrations (Throop and Lerdau 2004), thereby further
enhancing the quality of litter inputs to soil. As highlighted previously in this chapter,
such changes in organic matter input to soil typically promote the abundance of
microbes and animals in soil, and cause a shift to bacterial-based rather than fungal-
based soil food webs. This in turn can lead to a strong positive feedback on nitrogen
cycling and plant production, where the shift to bacterial-dominance enhances rates
of nitrogen mineralization which further promotes soil nitrogen availability and the
growth of competitive, fast-growing plant species (Fig. 3.22) (Welker et al. 2001). As
a result of this positive feedback on nitrogen cycling, it has been proposed that
ecosystem responses to nitrogen enrichment will be non-linear owing to plant species
replacements that cause enhanced nitrogen cycling, and will lead to increased
ecosystem nitrogen loss as a result of leaching (Welker et al. 2001). However, such
positive feedbacks on nitrogen cycling and plant production might also lead to greater
performance of invertebrate and vertebrate herbivore populations (Bowman 2000;
Van der Wal et al. 2003), which could stabilize or amplify shifts in vegetation
composition (Van der Wal et al. 2004; Van der Wal 2006). Also, the potential for
positive feedbacks on nitrogen cycling will depend on the capacity of ecosystems to

Disturbance, exhaustion of soil

Slow-growing, N deposition Fast-growing,

N-conserving species competitive species

Low rates of N cycling High rates of N cycling

High retention soil N High rates N leaching
Competitive displacement
from soils

Self- Self-
replacement replacement

Fig. 3.22 Conceptual model showing the generalized pattern of plant species self-replacement in
communities with low and high nitrogen availability. The model shows that in the face of greater
nitrogen deposition, nitrogen-conserving species of infertile environments will be replaced by more
competitive species, with traits that promote more rapid nitrogen cycling in soil. Under such
conditions, the new state would be preserved, even in the absence of additional N inputs, until
nitrogen reserves in soil are exhausted when species adapted to low nitrogen conditions will
re-establish. From Welker et al. (2001), with permission from Oxford University Press.
 3.6 Indirect effects of global change • 109

act as sinks for atmospheric nitrogen, thereby increasing the resilience of the system
to nitrogen enrichment (e.g. Aber et al. 1989; Zogg et al. 2000; Phoenix et al. 2004).
Experimental tests of the response of aboveground–belowground feedbacks to
nitrogen deposition are few, and complicated by the existence of strong direct effects
of nitrogen on the belowground subsystem, as discussed in Chapter 2. A study of
particular relevance is that of Manning et al. (2006), who designed an experiment to
tease apart the relative contributions of direct and indirect effects of elevated nitrogen
deposition on a suite of ecosystem properties. This study involved the setting up of
model plant-based ecosystems, and consisted of two factors, each with two levels, in
a factorial design. The first factor comprised low or high N deposition to detect direct
effects of nitrogen deposition on ecosystem functions. Meanwhile, the second factor
consisted of synthesized plant communities consisting entirely of plant species
characteristic of either high- or low-nitrogen-deposition environments. Using this
design, they were able to show that the response of model ecosystems to nitrogen
deposition was dominated by direct effects upon plant growth and soil biological
communities, rather than indirect effects that operated via differences in plant com-
munity composition. These effects appeared to be driven by the stimulation of plant
growth by nitrogen deposition, which increased litter inputs to soil and stimulated
decomposer biomass and activity in high-nitrogen microcosms. Although increased
litter inputs were associated with stimulated decomposer activity, this was insuffi-
cient to prevent the accumulation of carbon and nitrogen in soil of the high-N-
deposition treatment. The authors of this study took care to highlight that caution is
needed when extrapolating their results to field conditions. For example, some
possible compositional effects of elevated nitrogen, such as regional extinctions
and shifts in dominance of major plant functional groups, were not included in
their study. However, if similar results were to be obtained in natural ecosystems
then this would suggest that the direct effects of nitrogen deposition on ecosystem
function could in some circumstances be stronger than expected by indirect effects
manifested through changes in plant composition and diversity.
A recent study which sheds further light on the above issue is that of Suding et al.
(2008), who carried out a field study on alpine moist-meadow at Niwot Ridge,
Colorado, to examine the effects of species loss and nitrogen supply separately and
in combination on the vulnerability of the system to accumulated nitrogen. This was
tested by using combined treatments of removal of co-dominant plant species [the
forb Geum (formally Acomastylis) rossii, and the fast-growing grass Deschampsia
caespitosa] and manipulation of nitrogen supply over 6 years. They found that Geum
was associated with soil microbial feedbacks that slowed rates of nitrogen cycling,
while Deschampsia was associated with microbial feedbacks that increased rates of
nitrogen cycling. However, after 4 years of initial resilience to nitrogen supply, Geum
declined dramatically (by almost 70%) due to increasing nitrogen availability and
elimination of the soil microbial feedbacks, which in turn indirectly facilitated
Deschampsia via competitive release. Because Deschampsia was found to exert
strong competitive effects on subordinate plant species, it was concluded that this
increase in Deschampsia abundance might be accompanied by a community-wide
110 • 3 Plant influences and plant–soil feedbacks

drop in diversity. Interestingly, while some evidence of direct effects of enhanced

nitrogen supply were detected, such as a change in Geum cover, these effects were
relatively minor compared to the indirect effects mediated by interactions between
biota and resulting changes in nitrogen availability. This finding contrasts with
Manning et al. (2006) who found that direct effects of nitrogen addition on ecosystem
properties dominated over indirect effects in model systems. Suding et al. (2008) also
provide field evidence that plant–soil feedbacks through the microbial community
can influence vulnerability to nitrogen enrichment, and that responses to nitrogen
enrichment may be non-linear owing to plant species replacements that cause
enhanced nitrogen cycling.
Before leaving this topic, it is important to note that there is strong potential for
interactive effects between nitrogen enrichment and climate change on the below-
ground subsystem. As already mentioned, nitrogen enrichment can alleviate progres-
sive nitrogen limitation, which constrains the response of nitrogen-limited
ecosystems to elevated carbon dioxide concentrations (Luo et al. 2004). It may also
amplify climate-change-driven changes in vegetation composition, thereby increas-
ing the potential for indirect effects of vegetation change on the belowground
subsystem (Wookey et al. 2009). Also, as discussed in Chapter 2, nitrogen deposition
can have substantial effects on decomposition processes, thereby influencing the
response of soil respiration to warming and the capacity of soils to sequester carbon
under climate change (Davidson and Janssens 2006; Bardgett et al. 2008), for
example by suppressing decomposition and hence soil carbon loss (Craine et al.
2007; Reay et al. 2008). We therefore reiterate the case made in Chapter 2 that there is
an urgent need for experimental studies that consider simultaneous responses of
aboveground–belowground feedbacks to multiple global change drivers to improve
understanding of their effects on ecosystem-level processes under global change
scenarios.

3.7 Conclusions
In this chapter we have explored how aboveground communities affect the below-
ground subsystem, and how these effects in turn feed back aboveground. Some
aspects of this topic have attracted considerable attention over the past decade, and
there have therefore been several important advances in understanding. While it has
been long understood that plant species differ in their effects on the soil community
and the processes that they drive, we are now developing an improved mechanistic
and predictive understanding about why plant species effects differ, helped in a large
part by recognition that fundamental trait differences among species may have major
ecological consequences (Grime et al. 1997; Wardle et al. 1998a; Díaz et al. 2004;
Wright et al. 2004). Further, recent studies have shown that even within plant
communities there is huge trait variation among species (Hättenschwiler et al.
2008; Richardson et al. 2008), and that this trait variation may be much more
important than global variation in climate in driving microbial processes such as
 3.7 Conclusions • 111

plant litter decomposition (Cornelissen et al. 2007; Cornwell et al. 2008). Recent
studies have also focused on using community-weighted plant trait values to predict
aboveground and belowground ecosystem processes, pointing to the tractability in
some situations of being able to scale up from traits of individual leaves to processes
at the whole ecosystem level (e.g. Quested et al. 2007; Fortunel et al. 2009; but see
Wardle and Zackrisson 2005; Peltzer et al. 2009). Another important development is
the recognition that differences not just among species, but also within species may
be a powerful driver of the belowground system (e.g. Schweitzer et al. 2004; Classen
et al. 2007), and the intriguing suggestion has been made that different plant genes
or genotypes may be able to select for different soil communities, indicative of
‘community heritability’ (Whitham et al. 2003, 2008).
Another aspect of plant community effects on the belowground subsystem that has
attracted much recent attention is that of plant–soil feedbacks; that is, the notion that
plant species may select for soil communities that may either benefit themselves or
benefit other species. As such, a substantial number of plant–soil feedback studies
have appeared in the recent literature (Kulmatiski et al. 2008). Some recent studies
adopting this approach have proven their worth for understanding the role of plant–
soil feedbacks in influencing plant diversity (Packer and Clay 2000; Petermann et al.
2008), facilitating vegetation succession (De Deyn et al. 2003; Kardol et al. 2006),
and, as discussed in Chapter 5, driving plant invasibility. Much recent work has also
focused on improving our understanding of how human-induced global change
phenomena such as climate change and nitrogen deposition can influence the below-
ground subsystem through affecting both the performance of individual plants and
the functional composition of the vegetation. Recent studies have highlighted, for
example, that global change effects on feedbacks between the plant community and
the belowground subsystem have the potential to drive ecosystem processes that
influence ecosystem carbon flux (Wardle et al. 2003a; Cornelissen et al. 2007;
De Deyn et al. 2008; Chapin et al. 2009). Further, recent manipulative experiments
(e.g. Manning et al. 2006; Suding et al. 2008) are greatly enhancing our mechanistic
understanding the role of vegetation shifts and dominance in affecting soil commu-
nities and the processes that they drive under global change.
Despite significant recent activity in this topic, and increased understanding of it
on several fronts, there are many aspects that remain poorly understood and emerge
as important topics for future research. For example, while there is much understood
about how plant traits may drive aboveground–belowground linkages and feed-
backs, our knowledge of how plant traits select for traits of soil organisms and
vice versa lags well behind. Yet, such information is essential for developing a
mechanistic understanding of aboveground–belowground linkages that explicitly
incorporates the soil community, and how these linkages drive ecosystem processes.
Further, the relative importance of different routes through which plant communi-
ties affect the belowground subsystem is only starting to become explored. For
example, although the role of plant litter on the belowground subsystem has been
thoroughly investigated, we are only beginning to understand the ecological
importance of the immediate and much more rapid effects of live plant roots
112 • 3 Plant influences and plant–soil feedbacks

belowground (Pollierer et al. 2007; Högberg et al. 2008; Meier et al. 2009). Further,
our understanding of the relative importance of the direct versus indirect pathways
(Fig. 2.1) in driving plant–soil feedbacks is still relatively limited, largely because
most recent studies on plant–soil feedback have focused on grassland plants and
have employed methodologies that are likely to exaggerate the relative importance
of short-term feedbacks, especially those that involve pathogen build-up and
are often negative (Kulmatiski and Kardol 2008; Kulmatiski et al. 2008). Because
of the ease of applying these methods, recent research in this field is very uneven,
and more needs to be understood about the role of longer-term feedbacks (many of
which are positive), as well as the role of feedbacks in general in non-grassland
ecosystems.
Finally, studies on the effects of plant communities on the belowground subsystem
and feedbacks aboveground potentially provide us with useful tools for understand-
ing how global change phenomena affect ecosystems and fluxes of carbon between
the biosphere and the atmosphere. However, to move towards achieving this goal
requires focused effort on two questions that still remain relatively open. First, much
research is needed to understand how plant traits and feedbacks between plant and
soil communities influence the balance between ecosystem carbon gain and carbon
loss, and hence ecosystem carbon sequestration. Such information is essential for
predicting which ecosystems will gain or lose carbon under scenarios of global
environmental change. Second, we reiterate our point in Chapter 2, and that made
by Tylianakis et al. (2008), that the different global change drivers do not operate
independently of one another, and that our understanding of global change from an
aboveground–belowground perspective will be enhanced by studies that simultan-
eously consider multiple drivers.
4
Ecosystem-level significance of
aboveground consumers

4.1 Introduction
In the last two chapters we explored how biotic interactions between plant and
belowground communities act as drivers of terrestrial ecosystem functioning. We
also discussed the significance of aboveground–belowground relationships for under-
standing how global change phenomena affect processes at the ecosystem level,
especially in terms of the flux of carbon between the land and the atmosphere.
Ecological linkages between plant and belowground communities and their role in
regulating ecosystem functioning are also strongly affected by other trophic groups,
especially aboveground herbivores that consume plant material and initiate changes
in plant community structure and productivity, which propagate belowground
(Bardgett et al. 1998b; Bardgett and Wardle 2003; Wardle et al. 2004a). Moreover,
top predators can greatly alter the population density of herbivores and thus influence
their impacts on ecosystem processes (Post et al 1999; Terborgh et al. 2001, 2006). In
particular, effects of carnivores on ecosystem functions can be mediated through
changes in plant communities caused by altered herbivore abundance (Wardle 2002;
Thébault and Loreau 2003; Dunham 2008), and by shifts in foraging behaviour in
response to predation risk (Schmitz et al. 2004). Therefore, understanding the
ecological significance of herbivory for ecosystem functioning requires consideration
of their role in a multitrophic context, whereby herbivores and carnivores directly
and indirectly interact with plants to influence belowground biota and ecosystem
processes (Terborgh et al. 2001; Wardle et al. 2005; Dunham 2008; Schmitz 2008a).
Understanding the effects of herbivores and their predators on ecosystem pro-
cesses, however, is complicated because they involve a variety of mechanisms which
operate simultaneously over different temporal and spatial scales (Bardgett and
Wardle 2003). For example, the removal of plant shoot tissue by herbivores can
induce rapid changes in plant carbon and nitrogen allocation and root exudation
patterns, which as discussed in Chapter 3 can influence the growth and activity of
rhizosphere organisms that rely on carbon and other nutrients released from plant
roots (e.g. Guitian and Bardgett 2000; Hamilton and Frank 2001; Mikola et al. 2009).
At the same time, aboveground herbivory can induce a complex suite of chemical
changes in foliage, which impact on soil biota and rates of decomposition due to
altered litter quality (Bardgett and Wardle 2003). Over longer timescales, selective
114 • 4 Significance of aboveground consumers

feeding by herbivores or changes in foraging behaviour in response to predation risk

can cause shifts in plant community composition (e.g. Ritchie et al. 1998; Wardle
et al. 2001; Fornara and du Toit 2007), changing the amount and quality of litter
entering to soil and hence rates of decomposition and nutrient cycling (e.g. Pastor
et al. 1993; Wardle et al. 2001; Fornara and du Toit 2008). Added to this, animal
wastes (i.e. dung, urine, and insect frass) can create resource-rich patches in the soil
surface which influence the growth of plants, soil organisms and decomposition
processes (McNaughton et al. 1997a; Bardgett et al. 1998a; Frost and Hunter
2008a; Mikola et al. 2009). Further, disturbance by large herbivores can alter
soil physical properties, for instance through trampling and cultivation which can
negatively impact on soil organisms and processes of nutrient cycling (King and
Hutchinson 1976; King et al. 1976; Mikola et al. 2009). The relative importance
of these herbivore-mediated mechanisms relative to landscape factors varies tremen-
dously across ecosystems (Fig. 4.1), thereby causing differences in the scale and
direction of herbivore effects (Bardgett and Wardle 2003).
The goal of this chapter is to draw on the concepts developed in Chapters 2 and 3 to
outline how aboveground consumers, including herbivores and their predators, act as
drivers of ecosystem processes through their influence on soil biota and belowground
processes. There has been substantial progress in the last few years in understanding
the significance of the effects of aboveground consumers at the ecosystem level. First,
we synthesize what has been learned about the various mechanisms by which
herbivores can influence soil biota and ecosystem processes at the individual plant
and plant community level, and discuss how traits of plant species may have a role in
mediating herbivore effects on terrestrial ecosystem function. Second, we discuss the
influence of herbivores on belowground communities and ecosystem processes in a
multitrophic context, describing recent advances in understanding about how predator–
herbivore interactions and trophic cascades influence belowground properties and
the functioning of terrestrial ecosystems. Third, we describe recent studies which
demonstrate how aboveground biota move resources both within ecosystems and
across ecosystem boundaries, and discuss the consequences of this for the function-
ing of terrestrial ecosystems. Finally, we evaluate how aboveground consumers
might be indirectly influenced by global change through alteration of vegetation
productivity and composition, and how they might in turn modify responses of
terrestrial ecosystems to global change through their influence on plant and soil
communities.

4.2 Herbivore-mediated effects on plant–soil feedbacks

and ecosystem processes
Herbivores can have a wide range of effects on the functioning of terrestrial
ecosystems. Some of these effects are direct, involving the removal and consump-
tion of herbage (which can vary some 100-fold across terrestrial ecosystems),
trampling, and the return of animal excreta or insect frass (Floate 1981;
 4.2 Herbivore-mediated effects • 115

(a) (b)

(c) (d)

(e) (f)

Fig. 4.1 Fenced grazing exclosures erected across a range of ecosystems to study impacts of
herbivores on aboveground and belowground properties: (a) exclusion of sheep (Ovis aries)
grazing from hill grasslands in Llyn Llydaw, Snowdonia, Wales; (b) exclusion of sheep
(O. aries) from glacial outwash, Iceland; (c) exclusion of sheep (O. aries) grazing from
montane heath, Scotland; (d) exclusion of European red deer (Cervus elaphus) from regen-
erating birch (Betula pubescens) forest, Scotland; (e) exclusion of elk (Cervus canadensis),
bison (Bison bison), and pronghorn antelope (Antilocarpa americana) from grasslands at
Yellowstone National Park, USA; and (f) exclusion of reindeer (Rangifer tarandus) from
boreal forest with lichen (Cladina spp.) understorey in northern Finland. Photo credits: (a–d)
by R.D. Bardgett; (e) by D. Frank; (f) by D.A. Wardle.
116 • 4 Significance of aboveground consumers

McNaughton 1985; McNaughton et al. 1989; Bardgett and Wardle 2003; Frost
and Hunter 2008a). However, herbivores also have indirect effects on terrestrial
ecosystem functioning by modifying feedbacks between plants and soil biota
which influence rates of nutrient and carbon cycling (Bardgett et al. 1998b;
Bardgett and Wardle 2003; Wardle et al. 2004a). Such indirect effects of herbi-
vores on plant–soil feedbacks operate over different temporal and spatial scales,
ranging from short-term responses at the individual plant level to longer-term
responses at the plant community level, and can either accelerate or decelerate
rates of nutrient cycling (Ritchie et al. 1998; Bardgett and Wardle 2003; Wardle
et al. 2004a) (Fig. 4.2a). For instance, acceleration of nutrient cycles occurs when
herbivores promote the supply of labile substrates to soil as faeces and/or root
exudates, which stimulates soil decomposer activity, rates of nutrient mineraliza-
tion, and uptake of nutrients by grazed plants (Bardgett and Wardle 2003). In
contrast, deceleration of nutrient cycling occurs when selective feeding on nutri-
ent-rich plant species leads to the dominance of defended plants that produce poor
quality litter (Pastor et al. 1993; Ritchie et al. 1998), or when herbivory induces
the production of secondary metabolites in foliage which reduce litter quality and
decomposability (Rhoades 1985; Findlay et al. 1996) (Fig. 4.2b). In this section,
we provide an overview of some of the ways by which aboveground herbivory
can positively or negatively influence plant nutrition and productivity via changes
in belowground processes of decomposition and nutrient cycling. We illustrate
these pathways using specific examples from a range of ecosystems, thereby
providing a unifying perspective on herbivore effects on ecosystem processes
(Fig. 4.3).

4.2.1 Positive effects of herbivores on belowground properties and

ecosystem functioning
Positive effects of foliar herbivory on soil biota and nutrient cycling occur when
dominant plant species respond to grazing by exhibiting compensatory growth
(Augustine and McNaughton 1998). This pathway is most common in grasslands
where optimization of aboveground NPP by grazing mammals is often reported
(McNaughton 1985; McNaughton et al. 1997a; De Mazancourt et al. 1999). In
these situations, ungulate grazing positively affects the decomposer subsystem by
preventing colonization of later successional plants which produce poorer litter
quality, as well as through returning carbon and nutrients to the soil in labile forms
such as dung and urine, and as enhanced rhizodeposition (McNaughton et al. 1997a,
1997b; Bardgett et al. 1998a; Bardgett and Wardle 2003). Acceleration of nutrient
cycling by herbivores has also been reported in other ecosystems, including temper-
ate forests (Frost and Hunter 2008a), Arctic tundra (Van der Wal et al. 2004), and
boreal forest (Stark et al. 2000), albeit via different mechanisms. Moreover, the
ability of herbivores to accelerate soil nitrogen cycling has led to the suggestion
that they can alleviate nutrient deficiency and enhance their own carrying capacity
(McNaughton et al. 1997a).
 4.2 Herbivore-mediated effects • 117

(a) Acceleration effect

Herbivores

+
– Tolerant
plants
+ Intolerant
+
plants
Waste
products
Aboveground
productivity
+
N Supply

+
+ – Belowground
N Mineralization +
productivity

(b) Deceleration effect

Herbivores

–
+ High N
+ plants
Low nutrient
or chemically
Waste defended
products plants
Aboveground
+ productivity
–
N Supply
–
+ +

+ N Mineralization Belowground
productivity

Fig. 4.2 Feedback loops illustrating (a) the acceleration effect and (b) the deceleration effect of
herbivores on feedbacks between plant species and nutrient cycling. Arrows indicate net
indirect effect of herbivores on the abundance of plants or the rate of the process. From Ritchie
et al. (1998), with permission from the Ecological Society of American.

One of the most well-documented mechanisms by which herbivores promote

nutrient cycling is via the deposition of animal wastes, including urine, dung, and
insect frass. Herbivores consume and digest large quantities of aboveground plant
material, and nutrients can be released far more quickly into soil from the resulting
faeces than if released from litter. This in turn leads to increased nutrient availability
and plant nutrient uptake. In essence, this short-cuts the litter-decomposition
118 • 4 Significance of aboveground consumers

(a) FERTILE, PRODUCTIVE (b) INFERTILE, UNPRODUCTIVE

ECOSYSTEMS ECOSYSTEMS

HERBIVORES
High % of NPP consumed Low % of NPP consumed
High return of labile fecal material to soil Low return of fecal material to soil, high litter return
Cause retardation of succession, leading to Cause acceleration of succession, leading to
domination by plants with high litter quality domination by plants with low litter quality

PLANTS
Fast growing, short lived Slow growing, long lived
High allocation of C to growth High C allocation to secondary metabolites
High specific leaf area Low specific leaf area
Short leaf life span Long leaf life span
High forage quality Low forage quality

LITTER
High % N Low % N
Low phenolics High phenolics
Low lignin and structural carbohydrates High lignin and structural carbohydrates

SOIL FOOD WEB

Bacterial-based energy channel Fungal-based energy channel
High density earthworms High density enchytraeid worms
Relatively low density microarthropods High density macro-and microarthropods

SOIL PROCESSES
High bioturbation of soil Low soil mixing
Rapid decomposition and nutrient mineralization Slow decomposition and nutrient mineralization
Low soil C sequestration High soil C sequestration
High nutrient supply rates Low nutrient supply rates

Fig. 4.3 The difference in fundamental plant traits between species which dominate (a) fertile
systems that support high herbivory and (b) infertile habitats that support low herbivory
functions as a major ecological driver. This occurs through plant traits affecting the quality
and quantity of resources that enter the soil, and the key ecological processes in the decomposer
subsystem driven by the soil biota. These linkages between belowground and aboveground
systems feed back (dashed line) to the plant community positively in fertile conditions (a) and
negatively in infertile ecosystems (b). From Wardle et al. (2004a), with permission from the
American Association for the Advancement of Science.

pathway, and provides soil organisms with a highly decomposable resource that is
rapidly mineralized, thereby liberating nutrients for plant use. There are numerous
published studies of mammalian herbivore wastes stimulating soil microbial activ-
ity, nutrient cycling, and plant production. For example, in British hill grasslands,
urine and dung from grazing cattle and sheep are well known to increase soil
microbial activity and nitrogen cycling, leading to greater plant production in
grazed than ungrazed areas (Floate 1970a, 1970b; Bardgett et al. 1997, 2001b).
 4.2 Herbivore-mediated effects • 119

Also, in dry grassland and shrub-grassland at Yellowstone National Park, Frank

and McNaughton (1992) detected a positive association between dung deposition
and aboveground primary production, and suggested that grazing and productivity
are coupled to herbivore-facilitated nutrient cycling in this system. Likewise, Tracy
and Frank (1998) found that grazing by elk (Cervus canadensis), bison (Bison
bison), and pronghorn antelope (Antilocarpa americana) at Yellowstone National
Park caused increased soil microbial biomass and rates of nitrogen mineralization,
which was partly attributed to inputs of labile carbon from dung. In the Serengeti
National Park, Tanzania, McNaughton et al. (1997a, 1997b) found that urine from
gazelles enriched soils with nitrogen from urea, leading to a burst of organic-matter
mineralization, and in African savanna ungulate droppings accelerated nitrogen
mineralization in heavily grazed sites (Fornara and du Toit 2008). Further, in the
high Arctic Van der Wal et al. (2004) found that experimental addition of reindeer
(Rangifer tarandus) faeces to moss-dominated tundra increased soil microbial
biomass and grass growth, which again was attributed to increased nutrient avail-
ability (Fig. 4.4). It is important to note that herbivores can also change the spatial
distribution of nutrients within ecosystems through their dunging behaviour. For
instance, although rabbits deposit dung throughout their range, dung deposition is
higher in places where the animals congregate and a large amount of dung is
deposited in a small number of latrines (Willot et al. 2000). Consequently, soil
nitrogen availability in latrines is very high, despite high rates of nitrogen loss by
volatilization, leaching, and denitrification (Willot et al. 2000).
Although less studied, there is accumulating evidence that invertebrate herbivores
can also stimulate nutrient cycling and plant production. For instance, in a field
experiment, Belovsky and Slade (2000) found that grasshoppers enhanced soil
nitrogen cycling and plant abundance in prairie grassland. This was attributed in
part to grasshoppers preferentially feeding on plants of lower nitrogen content which
decompose slowly, thereby increasing the input to soil of litter from plants of higher
nitrogen content which decompose faster and therefore liberate more nutrients for
plant use. There is also evidence that waste from invertebrate herbivores (i.e. frass)
stimulates soil microbial activity and nitrogen cycling, thereby enhancing plant
production. For example, Frost and Hunter (2004) found that the addition of insect
frass to soils planted with red oak (Quercus rubra) saplings increased soil carbon and
nitrogen content, and caused a pulse in inorganic nitrogen availability and nitrogen
loss from soil in leachates. In a subsequent experiment, they added 15N-enriched
insect frass to mesocosms containing red oak saplings to follow the fate of frass-
nitrogen over 2 years (Frost and Hunter 2007). They found that while some of the
added frass-nitrogen was lost from soil in leachates immediately after addition, the
majority was retained in soil, which is consistent with the finding that the addition of
frass from larvae of the gypsy moth (Lymantria dispar) to soil stimulated microbial
growth and nitrogen immineralization (Lovett and Rueseink 1995), and with decidu-
ous forest soils being strong sinks for nitrogen inputs via microbial immobilization
followed by incorporation into organic matter (Zak et al. 1990; Zogg et al. 2000).
However, some of the added frass-nitrogen was also rapidly mineralized by soil
120 • 4 Significance of aboveground consumers

140
Shoot density

120 Mass per shoot

Above-ground biomass
100
Relative increase in fouled plots (%)

80

60

40

20

–20

–40
1998 1999 2000 2001

Fig. 4.4 Development of the response by grasses over 4 years to the addition of reindeer
(Rangifer tarandus) faeces in 1997 to moss-dominated tundra in high-arctic Spitsbergen,
measured as shoot density (no. m2), shoot mass (mg shoot1), and total aboveground live
mass of grasses (g m2). Data are expressed as the mean (+SE) increase in each of these
measures in fouled plots relative to the untreated control plots. Soil microbial biomass,
measured 4 years after the addition of reindeer feaces, was 85% greater in fouled areas than
the control. From Van der Wal et al. (2004), with permission from Wiley-Blackwell.

microbes, acquired by the oaks and recycled into foliage, and then assimilated by
late-season insect herbivores. Also, some of the frass-nitrogen taken up by the oaks
re-entered the soil system as leaf litter at the end of the first season, and was then
subject to decomposition processes in the following year. This latter finding indicates
that the effects of frass deposition can carry over and affect ecosystem processes
during decomposition. However, as shown by Frost and Hunter (2008a) in another
related study, these effects are short lived relative to abiotic forces which also regulate
decomposition process in forest soils. Collectively, these studies illustrate that, as
with ungulates, invertebrate herbivores can positively influence nutrient dynamics
and plant production in terrestrial ecosystems.
 4.2 Herbivore-mediated effects • 121

Another mechanism by which herbivory influences belowground processes is

via plant allocation. In particular, it has been shown that foliar herbivory of
grassland plants leads to short-term pulses in root exudation, which stimulate
the biomass and activity of microbes (Mawdsley and Bardgett 1997; Guitian and
Bardgett 2000; Hamilton and Frank 2001) and the abundance of their faunal
consumers (Mikola et al. 2001, 2009; Hokka et al. 2004; but see Ilmarinen et al.
2005). These positive effects of exudation on soil biota in turn have a positive
feedback to the plant through a temporary increase in soil nitrogen mineralization
and plant nitrogen acquisition, ultimately benefiting plant growth in the longer
term (Hamilton and Frank 2001; Hamilton et al. 2008; Sørensen et al. 2008)
(Fig. 4.5). Plant and soil responses to defoliation are known to vary across plant
species and with the timing and frequency of defoliation events (Guitian and
Bardgett 2000; Klironomos et al, 2004; Ilmarinen et al. 2005). However, the
ecological significance of these short-term responses to defoliation in grasslands
can be substantial, and it has been argued that they could explain, in part, the
compensatory response of grassland plants to ungulate grazing in natural ecosys-
tems (Hamilton and Frank 2001; Bardgett and Wardle 2003; Hamilton et al.
2008). Much less is known about the significance of defoliation-induced pulses
in root exudation in forest ecosystems, although pot experiments suggest that
exudation of carbon from tree roots is also important in mediating the response of
tree seedlings to herbivory (Ayres et al. 2004; Frost and Hunter 2008b). There-
fore, it is likely that carbon release from roots and its stimulatory impact on soil
microbes and nutrient availability is a widespread mechanism that enables plants
to compensate for loss of tissues through herbivory.
In the longer term, effects of herbivory on plant carbon and nitrogen allocation
become apparent through alterations in root biomass and nutrient content. There is

(a) (b) (c)

1.0 3 0.6
Potential net N mineralization
Soil NH4 +-N (mg/kg soil)

Soil NO3−-N (mg/kg soil)

(mg N. [kg soil]−1. day−1)

0.8 0.5

2 0.4
0.6
0.3
0.4
1 0.2
0.2
0.1

0.0 0 0.0
Unclipped Clipped Unclipped Clipped Unclipped Clipped

Fig. 4.5 Positive influence of defoliation of the grass Poa pratensis on soil nitrogen availability,
measured as: (a) soil NH4þ-N; (b) soil NO3-N; and (c) potential net nitrogen mineralization.
Values are means+1 SE in unclipped and clipped bulk soils (filled bars) and rhizospheric soils
(open bars) 24 h after treatment. This stimulation of soil nitrogen availability was in turn
associated with elevated plant nitrogen uptake, shoot nitrogen content, and rates of photosyn-
thesis. From Hamilton and Frank (2001), with permission from the Ecological Society of America.
122 • 4 Significance of aboveground consumers

mixed evidence about how herbivory affects root productivity, with positive (Milchunas
and Laurenroth 1993), negative (Guitian and Bardgett 2000; Mikola et al. 2001; Ruess
et al. 1998; Sankaran and Augustine 2004), and neutral (McNaughton et al. 1998)
effects being reported. Moreover, there appears to be no consistent relationships
between root responses to herbivory and rates of soil nutrient cycling. For example, in
a study on prairie dog colonies in Wind Cave National Park, South Dakota, grazing was
found to decrease the biomass and nitrogen content of roots, causing a reduction in
nitrogen immobilization due to reduced microbial growth, and an increase in net
nitrogen mineralization and plant nitrogen uptake (Holland and Detling 1990). In
contrast, in a study on temperate sub-humid grassland in Argentina, Chaneton et al.
(1996) found that grazing increased nitrogen allocation to roots, which increased root
biomass and the rate of underground nutrient circulation. In the Serengeti, increases in
nutrient cycling in response to herbivory have been found (McNaughton et al. 1997a),
despite there being no difference in root biomass between fenced and unfenced plots
(McNaughton et al. 1998).
Little is known about the relative importance of the main mechanisms described
above, namely animal waste deposition and defoliation, in explaining the effects of
herbivory on belowground organisms and nutrient cycling. However, a recent study
by Mikola et al. (2009) sheds some light on this issue. These authors examined the
relative importance of three grazing mechanisms, namely plant defoliation, dung and
urine return, and physical presence of herbivores (i.e. trampling and concentrated
dung and urine return), for explaining aboveground and belowground responses to
cattle in dairy pasture. They found that grazer effects on plant attributes, including
various measures of plant growth and nutrient allocation, were almost entirely
explained by plant responses to defoliation. However, for belowground attributes,
including the abundance of different faunal groups and soil nitrogen availability, the
picture was more mixed in that all mechanisms played a role, although dung and urine
return had major effects on soil animals and nitrogen availability when it was
concentrated in patches. This finding is consistent with that of Hamilton and Frank
(2001), who argued that animal wastes alone cannot explain the widely documented
positive effects of herbivores on grassland nutrient cycling at large spatial scales. This
is because, typically, waste patches remain localized within an ecosystem where
they greatly influence only a relatively small proportion of the total surface area
(Augustine and Frank 2001).
One final mechanism through which herbivores may positively affecting below-
ground processes is through modifying soil temperature. This mechanism appears to
be especially important in cold climes, such as the high Arctic where low soil
temperatures limit soil microbial activity and nutrient cycling (Brooker and
Van der Wal 2003). For example, grazing by barnacle geese (Branta leucopsis) and
reindeer in Ny-Ålesund, Spitsbergen, has been shown to reduce the thickness of the
moss layer, leading to an increase in soil temperature (Van der Wal et al. 2001).
Similarly, studies in the high Arctic of Spitsbergen, have shown that reindeer grazing
promotes soil nitrogen availability and plant productivity (Van der Wal et al. 2004),
partly as a result of reduced the depth of the moss layer in grazed areas (Brooker and
 4.2 Herbivore-mediated effects • 123

Van der Wal 2003). Studies on upland steppe in Yellowstone National Park (Coughenour
1991), seasonally dry high country in New Zealand (McIntosh et al. 1997), and oak
savanna in Minnesota (Ritchie et al. 1998), have also reported positive effects of
herbivory on soil temperature. This may potentially contribute to the acceleration of
decomposition and nitrogen mineralization in these situations, at least if increased
soil temperature is not accompanied by a loss in soil moisture.

4.2.2 Negative effects of herbivores on belowground properties and

ecosystem functioning
One of the main routes by which herbivores negatively affect nutrient cycling and
plant production is through selective foraging on nutrient-rich plants. This is
especially prevalent in relatively unproductive and infertile ecosystems, where
low rates of consumption and selective foraging on the most nutritious plant species
with the highest litter quality lead to the dominance of well-defended plants that
produce recalcitrant litter (Ritchie et al. 1998). Because most nutrients are returned
to the soil as plant litter in these situations, the net effect of herbivory is to reduce
soil biotic activity, nutrient mineralization, and supply rates of nutrients to plants,
and this overrides any positive effects of dung and urine (Fig. 4.2b) (Bardgett and
Wardle 2003). A classic example of the importance of selective feeding by herbi-
vores for soil processes is the study of Pastor et al. (1993) on moose (Alces alces)
browsing in the boreal forests of the Isle Royale National Park, Michigan, USA.
These authors showed that selective foraging by moose on deciduous hardwoods,
with nutrient-rich foliage, led with time to dominance by less nutritious species
such as spruce which produces litter of lower quality and hence decomposability.
This slow-decomposing litter in turn accumulates on the soil surface, leading to a
reduction in soil nitrogen mineralization and hence a decline in the productivity of
the ecosystem (Fig. 4.6).
Several other studies across a range of ecosystems also report that selective
foraging increases the dominance of less nutritious species that ultimately slow
down the rate of nutrient cycling. For example, Ritchie et al. (1998) found that
selective foraging by deer, rabbits, and a variety of insects in oak savanna in
Minnesota decreased rates of nutrient cycling rates due to the removal of nutrient-
rich woody plants and legumes. This in turn led to dominance by prairie grasses
(e.g. Andropogon geradi and Sorghastrum nutans) that produce nutrient-poor
litter of low decomposability, thereby slowing down rates of nutrient cycling.
Likewise, Van Wijnen and Van der Wal (1999) found that grazing by geese,
hares, and rabbits in salt marsh encouraged domination by nutrient-poor and
tannin-rich plants such as common sea lavender (Limonium vulgare). The litter
produced by this species decomposes slowly, impairing rates of nutrient miner-
alization. Similarly, Kielland and Bryant (1998) found that selective browsing by
moose in Alaskan taiga led to the replacement of nutritious deciduous tree species
by less nutritious evergreens with recalcitrant litter, thereby slowing down rates of
nutrient turnover. Finally, Harrison and Bardgett (2004) found that selective
124 • 4 Significance of aboveground consumers

Increased consumption by moose

Selective browsing on
hardwoods

Reduced tree production due to shift to

conifer (spruce) dominance

Decreased leaf litter quality

(+% cellulose/–% N)

Proportional decline

Reduced soil microbial activity and N

mineralization

Not compensated by
priming effect of faeces

Reduced productivity of ecosystem

Moose consumption
exceeds browse supply

Collapse in moose population

Fig. 4.6 Schematic diagram of the cascading effects of moose (Alces alces) browsing on
ecosystem properties in the Isle Royale National Park, Michigan. Adapted from Pastor et al.
(1993) by Bardgett (2005), and reproduced with permission from Oxford University Press.

browsing and the consequent reduction in growth of the dominant tree species
Betula pubescens by European red deer (Cervus elaphus) in regenerating forest in
the Scottish Highlands reduced rates of soil nitrogen mineralization (Fig. 4.7).
This arises through the well-known ability of B. pubescens to positively affect
soil nutrient cycling through improvements in the quality of litter inputs to soil
and by the action of its roots. However, this increase in nitrogen mineralization in
unbrowsed plots was not matched with an increase in soil phosphorus availability,
and therefore led to a shift from nitrogen to phosphorus limitation of tree growth
(Carline et al. 2005).
In situations where shifts in plant community composition resulting from select-
ive grazing slow down rates of nutrient cycling, a feedback system may subse-
quently emerge. Here, reduced rates of nutrient cycling and availability will further
favour the growth of nutrient-poor species that have high nutrient-use efficiency,
 4.2 Herbivore-mediated effects • 125

N mineralization (mg N m2 day)

120

100

80

60

40
Browsed Unbrowsed
Treatment

Fig. 4.7 Negative effect of red deer (Cervus elaphus) browsing on rates of soil nitrogen
mineralization in regenerating birch forest at Creag Meagaidh National Nature Reserve in the
Scottish Highlands. From Harrison and Bardgett (2004), with permission from Elsevier.

thereby enhancing their competitive dominance in nutrient-poor habitats. Such a

feedback strengthens the effects of the herbivores on the ecosystem and could lead
to additional reductions in plant production and rates of nutrient cycling (Ritchie
et al. 1998). However, it should be noted that herbivore-induced shifts in vegetation
composition that favour of nutrient-poor plants do not always result in reduced rates
of nutrient cycling. For example, Wardle et al. (2001) sampled soils from inside and
outside fenced enclosures across 30 locations in New Zealand forests, and found
that while browsing by introduced mammals (feral goats and deer) altered vegeta-
tion in a consistent way (reducing nutritious broad-leaved species and promoting
other less nutritious types), subsequent effects on measures of soil nutrient status
were highly idiosyncratic, with an equal number of positive and negative effects
being detected. Moreover, effects of herbivory on vegetation composition, and
hence feedbacks to soil nutrient cycling, also appear to depend on soil fertility
itself. For example, Buckland and Grime (2000) found by using synthesized plant
communities that under low-fertility conditions preferential feeding by inverte-
brates on nutrient-rich early successional species accelerated vegetation succession
and the growth of late successional plant species known to produce poorer-quality
litter. In contrast, under fertile conditions herbivory retarded vegetation succession
and led to the dominance of early-successional nutrient-rich species (presumably
because their main defence against herbivory is rapid compensatory growth that is
made possible by high resource availability) (Buckland and Grime 2000). Although
they did not assess the consequences of these plant community changes for the
belowground subsystem, it is likely that acceleration of vegetation succession under
infertile conditions will have further reduced soil nutrient availability and therefore
strengthened the dominance of nutrient-poor, late-successional species that thrive
under these conditions. In contrast, the retardation by herbivores of succession
126 • 4 Significance of aboveground consumers

under more fertile conditions and the continued dominance of fast-growing nutrient-
rich plant species would be expected to further promote soil fertility and the
dominance of nutrient-rich species.
Another mechanism through which herbivores could contribute to the slowing
down of nutrient cycling is the promotion of plants that accumulate secondary
metabolites within their leaves, which in turn reduces plant litter quality and thereby
adversely affects the soil biota and its activity. Some plant species can produce a vast
cocktail of secondary metabolites, and many of these chemicals are known to have
adverse effects on herbivores through a variety of mechanisms (Hartley and Jones
1997). As such, these plant species are often avoided by herbivores, which can then
dominate the plant community (Bardgett and Wardle 2003). Further, herbivore
attack, especially by invertebrates, is well known to induce the production by plants
of secondary metabolites that serve as defence compounds (Schultz and Baldwin
1982; Rhoades 1985; Agrawal et al. 1999; Nykanen and Koricheva 2004), with
subsequent impacts on the herbivores themselves (Wold and Marquis 1997; Boege
2004). Few studies have studied the after-life effects on decomposition and nutrient
cycling of herbivore-induced changes in plant secondary metabolite production.
However, Findlay et al. (1996) found that cellular damage caused by spider mites
to seedlings of eastern cottonwood (Populus deltoids) increased the concentration of
polyphenols in foliage, resulting in a 50% reduction in the rate of decomposition of
subsequently produced leaf litter. Also, it is well established that plant secondary
metabolites such as polyphenolics can play an important role in terrestrial-ecosystem
nutrient cycling (Hättenschwiler and Vitousek 2000), for example through reducing
rates of nitrogen fixation (Schimel et al. 1998), nitrification (Baldwin et al. 1983), and
nitrogen mineralization (Northup et al. 1995). Consequently, it is reasonable to
assume that increased production of plant secondary metabolites following herbivore
attack will reduce the quality of litter inputs to soil, their decomposability, and hence
rates of nutrient cycling.
So far, we have considered how herbivores can reduce of rates of nutrient cycling
through altering the quality of litter inputs to soil. However, reductions in NPP and
hence the quantity of organic matter entering soil also has the potential to negatively
influence soil biota and the functioning of the belowground subsystem. For example,
Sankaran and Augustine (2004) showed that grazing by large mammals in a semiarid
grassland ecosystem in Kenya reduced soil microbial biomass in both high- and low-
fertility sites. This was likely due to reductions in plant carbon input to soil resulting
from a depression in root production, as well as the diversion of plant carbon to
herbivore respiration and growth. Likewise, the previously mentioned negative
effects of browsing by red deer (C. elaphus) on soil nitrogen cycling in regenerating
forest reported by Harrison and Bardgett (2004) were in part attributed to a reduction
in the growth of the dominant tree species B. pubescens (Fig. 4.7), and hence the
amount of carbon entering soil from its roots and foliage. These examples contrast
with studies of productive grasslands, where herbivore-mediated increases in
primary productivity have been shown to enhance carbon addition to soil, thereby
stimulating soil biological activity because it alleviates carbon limitation of microbes
 4.2 Herbivore-mediated effects • 127

(Bardgett and Wardle 2003). However, it is important to note that knock-on effects
of herbivore-induced changes in NPP to the belowground subsystem and nutrient
cycling are not at all clear. For example, increasing NPP has been shown to have
both positive and negative effects on both microbial biomass and higher trophic
levels of the soil food web (Chapter 3; see also Wardle 2002). There are two reasons
for such contrasting responses: first, the relative importance of top-down and bottom-
up forces in regulating soil food web components may be context-dependent; and
second, plants not only provide carbon resources for microbes but also compete with
them for nutrients. Therefore, the direction of effects of herbivore-induced changes
in NPP on the belowground subsystem may be governed by which of two opposing
effects (stimulation of microbes by carbon addition, inhibition of microbes by
resource depletion) dominates.
It should be noted that not all soil organisms are stimulated by enhanced carbon
input to soil, such as occurs following defoliation. In particular, the growth of
mycorrhizal fungi is often reduced following defoliation because carbon is prefer-
entially allocated to other plant and soil pools (Gehring and Whitham 1994, 2002).
Evidence for this arises from a literature synthesis by Gehring and Whitham (1994)
which revealed that mycorrhizal colonization declined following defoliation or
grazing by ungulates for 23 of the 37 plant species that had been examined at
that time, whereas it was unaffected for ten species, positively affected for two
species, and showed variable responses for two species. Moreover, the widely
reported negative relationship between mycorrhizae and herbivory was found to
occur across a wide range of plant types, including grasses colonized by arbuscular
mycorrhizal fungi and conifers colonized by ectomycorrhizal fungi (Gehring and
Whitham 1994). As emphasized by Gehring and Whitman (1994), however, it is
difficult to draw firm conclusions on this topic because studies examining the
effects of herbivory on mycorrhizal fungi are limited in number and scope, and
cover only a small number of plants in a limited range of environments. Also, more
recent studies indicate that it is difficult to generalize about the response of fungal
symbionts to defoliation, in that responses vary with the frequency (Klironomos
et al. 2004) and timing (Saravesi et al. 2008) of defoliation. Further, effects of
defoliation on mycorrhizal fungi are not restricted to changes in root colonization,
because other fungal structures such as vesicles, spores, and extra-radical hyphae of
arbuscular mycorrhizal fungi (Klironomos et al. 2004), and sporocarps of ectomy-
corrhizal fungi (Kuikka et al. 2003), are also affected. Clearly further studies are
needed to determine the ecological significance of such herbivore-induced changes
in mycorrhizal communities and to test for generalities in responses across a range
of plant species and environmental conditions.
One further mechanism by which herbivores can negatively impact soil biota and
nutrient cycling is via physical disturbance, which is commonly associated with
intensive grazing. This has been most widely documented in livestock farming
systems, where high grazing pressures can lead to soil compaction, erosion, and
poaching of the soil surface, with negative impacts on soil biota and ecosystem
productivity. For example, increased livestock stocking densities on pasture have
128 • 4 Significance of aboveground consumers

been found to severely reduced collembolan numbers in the surface soil due to soil
compaction and associated reductions in soil pore space (King and Hutchinson 1976;
King et al. 1976; Walsingham 1976). Further, simulated cattle trampling was found to
strongly reduce the abundance, diversity, and species richness of oribatid mite and
Collembola communities in grassland (Fig. 4.8) (Cole et al. 2008). Over longer time
scales, there are numerous reports in the literature of overgrazing causing catastrophic
soil degradation, especially in the world’s drylands which are especially prone to
desertification (Diamond 2005; Avni et al. 2006; Lal 2009). For instance, in the African
Sahel, overgrazing by cattle has caused a catastrophic shift to a desertified ecosystem
state that can no longer sustain livestock production (Rietkerk et al. 2004), and in the
Negev Highlands, Israel, the overgrazing caused by local Bedouin population has
accelerated the soil-degradation process (Avni et al. 2006).
Reports of herbivore-driven physical disturbance are also common in natural
ecosystems. For example, increased grazing by lesser snow geese (Anser caerules-
cens caerulescens) along the coast of the Hudson Bay, Canada, has promoted
hypersaline conditions due to enhanced soil evapotranspiration, which has caused
the destruction of salt marshes and subsequent eviction of its grazers (Jefferies
1998; Srivastava and Jefferies 1996). Likewise, in the high Arctic at Svalbard,
spring foraging by pink-footed geese (Anser brachyrhynchus) for belowground
plant parts, such as rhizomes, roots, and tubers (termed grubbing), is associated
with significant disturbance to vegetation and soil, causing localized declines in
plant cover, carbon uptake, and soil carbon storage (Fig. 4.9) (Van der Wal et al.
2007). The main concern here, however, is that the pink-footed goose population
has doubled over the last 30 years (Fox et al. 2005), and is expected to increase
with climate warming (Jensen et al. 2008), potentially causing widespread vegeta-
tion loss and soil disturbance in the European Arctic (Speed et al. 2009). Further,
high levels of grazing pressure by reindeer in dry boreal forest in Fennoscandinavia
have been associated with the removal of lichen cover, which exposes soil biota to
a less favourable microclimate (Stark et al. 2000), and with soil compaction and the
crushing of plant roots, which reduces carbon supply to soil (Stark et al. 2003).
While these responses to grazing are likely to have negative consequences for
nutrient cycling, the net effect of reindeer grazing will depend on the relative
dominance of negative and positive effects of grazing, which could also vary
depending on season (Stark et al. 2000, 2003). However, a study by Sørensen
et al. (2009) found that the effects of simulated reindeer trampling on decomposer
communities in sub-Arctic grasslands outweighed the effects of defoliation and
fertilization by reindeer. These authors also found that simulated trampling nega-
tively affected the coverage of mosses and sedges, as well as the abundance
of functionally important faunal groups such as collembolans and enchytraeids.
Finally, as discussed in Chapter 5, physical disturbances propagated by invasive
herbivores such as pigs (Sus scrofa) and beavers (Castor canadensis) can greatly
transform ecosystems, leading to potentially substantial changes in soil organisms
and processes.
 4.2 Herbivore-mediated effects • 129
(a)
40000 b
35000 b
30000 a
Density (m–2)

25000 a
a a a
20000
a
15000
10000
c
5000
0
0 50 100
(b)
2.5

a a
2
b
Diversity index

b b b b b
1.5
c

0.5

0
0 50 100
(c)
12
a
10 a
b
Species richness

8 b
b
b b
6 bc c

2
0
0 50 100
Disturbance (%)

Fig. 4.8 Response of oribatid mites (open bars), mesostigmatid mites (shaded bars), and
Collembola (hatched bars) to disturbance caused by simulated cattle grazing in grassland.
The disturbance levels refer to 0, 50, and 100% ground-cover disturbance and data are for
(a) abundance, (b) diversity (Shannon–Wiener diversity index), and (c) richness of species to
these disturbance treatments. Error bars represent SE and bars within the same panels bearing the
same letter do not differ at P < 0.05. From Cole at al. (2008), with permission from Elsevier.
130 • 4 Significance of aboveground consumers

(a) (b)
Vascular plants
5000
Moss
4000

Stored carbon (g m–2)

Organic horizon

3000

2000

1000

0
Control Grubbed

Fig. 4.9 (a) Spring foraging by pink-footed geese (Anser brachyrhynchus) for belowground
plant parts, such as rhizomes, roots, and tubers (termed grubbing), is associated with
(b) significant disturbance to vegetation and soil, causing localized declines in soil carbon
storage in the high Arctic. The data show that the amount of carbon stored in the surface
organic horizon of the soil was reduced by goose grubbing. From Van der Wal et al. (2007) and
image by Christiaane Gruss, with permission from Wiley-Blackwell.

Before leaving the topic of physical disturbance, it is important to note that, in most
cases, the detrimental effects of intensive grazing are localized in both space and
time. For instance, grubbing by pink-footed geese in the high Arctic is most intense in
early spring when they migrate from their southern wintering grounds, and in wetter
habitats in low-lying landscapes where their preferred forage is abundant (Speed et al.
2009). However, it is likely that increased disturbance of preferred habitats by these
geese will force them to forage less preferred habitats, thereby extending their impact
to the landscape scale with far-reaching implications for ecosystem functioning
(Speed et al. 2009). Likewise, in grazed pastures, excessive trampling and associated
loss of vegetation cover tends to occur in localized areas, for instance around
supplementary feeding areas, gates and walkways, and at times of excessive soil
wetness. However, as will be considered later in this chapter, predicted increases in
grazing pressures due to climate or land use change will increase both the temporal
and spatial extent of grazing, potentially leading to large-scale vegetation loss and
soil disturbance in natural ecosystems (van de Koppel et al. 2005; Speed et al. 2009).

4.2.3 Landscape-scale herbivore effects and multiple stable states

Although herbivores have a great ability to modify ecosystems via the mechanisms
described above, their effects on ecosystem processes are in some cases outweighed
by landscape controls, such as spatial variation in topography, soil texture, and soil
moisture conditions. For example, in the aforementioned study of regenerating forest
in Scotland, Harrison and Bardgett (2004) found, using four fenced exclosure plots,
 4.2 Herbivore-mediated effects • 131

that although browsing by red deer had significant and negative effects on measures
of soil biological properties and nitrogen cycling, the topographic position of the
exclosures was the dominant factor affecting these measures at the landscape scale.
Likewise, studies of grazer effects in native grassland at Yellowstone National Park
revealed that topographic position, and associated variation in soil conditions, was
often the dominant factor affecting soil biological properties and rates of nutrient
cycling (Tracy and Frank 1998; Verchot et al. 2002). Also, in the previously men-
tioned study by Sankaran and Augustine (2004), landscape-scale constraints on soil
organic matter content were found to overarch the negative effects of grazers on
microbial abundance. Further, in sub-Arctic grassland in Abisko, northern Sweden,
local-scale variation in soil abiotic properties was shown to have a stronger impact on
soil biota than did simulated reindeer grazing (Sørensen et al. 2009).
At the landscape scale, herbivore impacts are also likely to vary substantially
across environmental gradients of soil fertility, topographic position, and climate
(Olff and Ritchie 1998; Olff et al. 2002; Anser et al. 2009). For example, using an
airborne remote-sensing system, Anser et al. (2009) showed that the impact of
large herbivores (including elephants, buffalo, giraffe, and zebra) on vegetation
structure in the Kruger National Park, South Africa, varied by topographic pos-
ition, geologic substrate, and time since grazing was excluded. In particular, they
found that effects of herbivore exclusion on woody vegetation structure were
greater on nutrient-rich clay soils formed on basalt substrate than on sandy soils
formed on granite, and in lowland (where water, nutrients, and hence forage are
locally abundant) than upland areas. Similarly, Augustine and McNaughton (2006)
found in Kenyan rangeland that the effects of grazers (including impala, zebra, and
buffalo) on plant production and nitrogen cycling varied with both soil fertility and
with annual rainfall patterns. They found that in low-rainfall years grazers reduced
aboveground plant production in both high- and low-fertility sites. However, in a
high-rainfall year grazers enhanced aboveground plant production and soil nitrogen
availability in high-fertility sites, but suppressed these properties on low-fertility
sites. These findings not only indicate that grazer effects on aboveground plant
production and nitrogen cycling are tightly coupled at the landscape scale, but also
that climatic variability is an important determinant of grazer effects in grassland
systems.
Effects of herbivores can also vary greatly in space and time depending on
population fluctuations and herbivore body size (Bakker et al. 2004). For example,
the scale of redistribution of nutrients (discussed later in this chapter) and the
feeding behaviour of herbivores, as well as the extent to which they influence
soil physical properties, is body-size-dependent (Olff and Ritchie 1998; Bakker
et al. 2004). As a consequence, different-sized herbivores have the potential to have
different effects on soil nutrient cycling in the same habitat, but at different
temporal and spatial scales. Very few studies have explored these issues, although
Bakker et al. (2004) used an exclosure set-up in grassland grazed by cattle, rabbits,
and meadow voles, in which fences with different hole sizes were used to select-
ively exclude different components of the grazing herbivore community based on
132 • 4 Significance of aboveground consumers

body size. They found that that exclusion of cattle grazing led to a 1.5-fold increase
in net nitrogen mineralization, which was attributed to a build-up of litter on
the soil surface. In contrast, the combined exclusion of cattle and rabbit grazing
(i.e. vole grazing only) altered the timing of N cycling, causing an autumn maxima
in nitrogen mineralization which coincided with a peak in vole density and high
levels of N input through vole faeces. In general, very little is known about how
herbivore population dynamics and life histories impact on nutrient cycling at the
landscape-scale or their importance relative to abiotic controls on ecosystem pro-
cesses, such as topography, soil fertility, and climate. Future studies on these topics
are therefore required to fully understand how the types of herbivore effects that
have been well studied at local spatial scales on ecosystem processes are mani-
fested at the landscape scale.
One area that has received recent attention is the idea that gradual changes in
ecosystems resulting from herbivory can lead to dramatic stepwise transitions, or
alternative stable states (Rietkerk and van de Koppel 1997; van de Koppel et al.
1997; Rietkerk et al. 2004; Van der Wal 2006). Consequently, ecosystems can
contain mosaics of communities in several alternative states which are each
relatively resistant to change, but can exhibit rapid shifts to another state if subject
to altered grazing pressure. The concept of alternative stable states has been applied
to situations where overgrazing has led to soil degradation and an associated
complete and irreversible collapse in existing vegetation, and ultimately the for-
mation of a two-phase mosaic consisting of patches of dense vegetation alternating
with almost bare areas (McNaughton 1983; Belsky 1986; Rietkerk and van de
Koppel 1997; van de Koppel et al. 1997). For instance, overgrazing in semi-arid
ecosystems in the Sahel region of Africa, and resultant soil erosion, compaction,
reduced infiltration, and increased water runoff, has been shown to trigger cata-
strophic shifts from a highly productive vegetated state to a severely degraded state
(Fig. 4.10) (Rietkerk et al. 1997; Rietkerk and van de Koppel 1997). Similar
mosaics have also been reported in Arctic coastal plant communities in Hudson
Bay, where summer grazing by geese creates grass-dominated grazing lawns, while
spring grubbing for roots and rhizomes causes destruction of existing plant com-
munities and the creation of patches of bare ground with reduced nutrient avail-
ability that are slow to recover (Jefferies 1998; Srivastava and Jefferies 1996).
It has been argued that improved understanding of such herbivore-driven alterna-
tive stable states could help to establish whether an ecosystem might collapse under
certain conditions, or whether there are warning signs of imminent collapse
(Rietkerk and van de Koppel 1997).
Although typically associated with overgrazing, the alternative stable states frame-
work has also been applied to evaluate non-degenerative herbivore-driven vegetation
change, especially in tundra ecosystems. As argued by Van der Wal (2006), the
Arctic tundra can occur in essentially three different vegetation states, and relatively
sudden transitions between them are driven by reindeer grazing: one is characterized
by lichen dominance, one by moss dominance, and one by an abundance of
graminoids. Importantly, herbivore-driven transitions from lichen-dominated to
 4.2 Herbivore-mediated effects • 133

Equilibrium plant density sta

ble
equ
ilib
riu
m

oints
breakp

Level of herbivory

Fig. 4.10 A catastrophic fold showing the relationship between equilibrium plant density and
the level of herbivory. Sudden jumps in plant density occur at distinct levels of herbivory,
leading to catastrophic shifts from a highly productive vegetated state to a severely degraded
state. From Rietkerk et al. (1997), with permission from Wiley-Blackwell.

moss- and graminoid-dominated states are associated with increases in plant prod-
uctivity and hence the carrying capacity for reindeer populations (Fig. 4.11). This
idea is consistent with the classic work of Zimov et al. (1995), described in Chapter 5,
which proposes that the extinction of mega-herbivores at the end of the Pleistocene
was responsible for a large-scale biome shift from productive grass-dominated
steppe to unproductive moss-dominated tundra across Alaska and Russia. However,
as documented by Van der Wal (2006), the more recent expansion of reindeer across
the Arctic provides yet more evidence that herbivores are responsible for sudden
shifts between the three vegetation states that enhance their carrying capacity. For
example, grazer-driven switches from lichen to moss-dominated vegetation (caused
primarily by selective grazing and trampling) have been reported in Greenland
(Thing 1984), Svalbard (Cooper and Wookey 2001; Van der Wal et al. 2001), Russia
(Vilcheck 1997), and North America (Manseau et al. 1996), allowing tundra to
sustain a greater density of reindeer (Van der Wal 2006). Also, there are many
reports across the Arctic of intensive reindeer grazing causing a transition from
moss- to graminoid-dominated tundra (Olofsson et al. 2004; Van der Wal and
Brooker 2004; Van der Wal et al. 2004), which as already discussed in section
4.2.1 is associated with plant–soil feedbacks that enhance soil nitrogen cycling and
plant productivity (Van der Wal et al. 2004), enhancing the carrying capacity of the
ecosystem. What is clear from these examples is that herbivores have the capacity to
force sudden and predictable shifts in vegetation state within terrestrial ecosystems,
with both catastrophic negative (Rietkerk and van de Koppel 1997; van de Koppel
et al. 1997) and positive (Van der Wal 2006) consequences for their functioning and
carrying capacity.
134 • 4 Significance of aboveground consumers

Tundra vegetation state

Total plant productivity Lichen-dominated Moss-dominated Graminoid-dominated

Grazing pressure

Fig. 4.11 Schematic representation of the occurrence of tundra vegetation states in relation
to grazing pressure exerted by reindeer or caribou (Rangifer tarandus). Herbivore-driven state
transitions from lichen- to moss- and graminoid-dominated state are associated with an increase
in plant productivity and carrying capacity for reindeer populations. From Van der Val (2006),
with permission from Wiley-Blackwell.

4.3 The role of plant traits in regulating

herbivore impacts
As discussed in Chapter 3, plant traits provide a framework for understanding how
changes in vegetation composition and diversity influence belowground communities
and the ecosystem processes that they drive. Given that grazing is both dependent on,
and influences, plant functional traits (Huntly 1991; Díaz et al. 2006), an understand-
ing of plant trait responses to grazing helps provide a framework for investigating
feedbacks between grazers, plants, soil organisms, and nutrient cycles, as well as how
they vary across environmental gradients such as soil fertility and climate.
Although most studies on herbivore effects of vegetation do not explicitly consider
plant traits, conceptual models of plant trait responses to grazing do exist (e.g. Diaz
et al. 2006). For example, the range-succession model predicts that grazing increases
the cover of annual plants over perennials, leads to the replacement of palatable by
unpalatable plants, and causes replacement of tall grasses by short grasses, shrubs,
and prostrate herbs (Dyksterhuis 1949; Arnold 1955). Likewise, when adapted to
consider responses to grazing, Westoby’s (1998) LHS (leaf-height-seed) model
predicts that moderate, selective grazing promotes plants with a particular set of
 4.3 Plant regulation of herbivore impacts • 135

traits linked to unpalatability, whereas heavy, non-selective grazing promotes

plants with traits associated with palatability. Other models distinguish plant trait
responses to grazing in productive and less-productive ecosystems, where the
proximate cause of variation in productivity is water and nutrient availability. For
instance, the generalized model of Milchunas et al. (1988) predicts that plant trait
responses to grazing depend on rainfall (as a proxy for productivity) and grazing
history, and are the most marked in humid (productive) systems with a long grazing
history where short annual plants with prostrate growth are encouraged. Likewise,
models such as those proposed by Grime (1977) and Coley et al. (1985) predict that
plant trait responses to grazing depend on productivity, in that grazing promotes
palatable plants (i.e. those with high grazing tolerance, involving fast re-growth of
high-quality tissue and low investment in structural defence) in humid situations,
and unpalatable plants (i.e. those with grazing avoidance, involving slow-growing
tissue and high investment structural defence) in dry systems. Moreover, as sug-
gested by Herms and Mattson (1992), grazing history also plays an important role:
the stronger the historical impact of grazing, the stronger the selection for plants
that have traits associated with investment in grazing avoidance.
In order to determine whether some widely recognized plant trait responses to
grazing are consistent at the global level, Díaz et al. (2006) performed a meta-
analysis of 197 studies selected from around the globe. In this synthesis, they found
that grazing favoured annual over perennial plants, short over tall plants, prostrate
over erect plants, and plants with stoloniferous and rosette architecture over
tussocks. Also, and consistent with the models mentioned above, they found that
grazing consistently favoured plants with traits that confer low palatability, and
that this response was strongest in dry systems with a long grazing history. An
important finding of Díaz et al. (2006) was that in almost all cases that they studied
the response of plant traits to grazing varied depending on both climate and grazing
history, suggesting that vegetation responses to grazing are modulated by these two
factors. This finding has important consequences for understanding grazer effects
on belowground properties and nutrient cycles at the global scale, given the strong
link between plant traits and the belowground subsystem discussed in Chapter 3.
However, as noted by Díaz et al. (2006) our knowledge of the effect of grazing is
restricted to a surprisingly small number of plant traits, and data availability varies
markedly across regions, making it difficult to generalize too much about plant
responses to herbivory across gradients of climate, grazing history, and soil
fertility.
Although the above models and literature synthesis of Díaz et al. (2006) do not
explicitly consider cascading effects of grazing on the belowground subsystem and
nutrient cycling, they provide a very general framework for understanding variation
in grazer impacts belowground across ecosystems of differing fertility and precipita-
tion regimes. While the magnitude and direction of herbivore effects on the below-
ground biota, nutrient dynamics and plant production differs greatly across
ecosystems (Bardgett and Wardle 2003), this variation appears to depend largely
on ecosystem productivity in a way that is broadly consistent with the models of plant
136 • 4 Significance of aboveground consumers

trait responses discussed above. For instance, positive effects of grazing on soil biota
and nutrient cycling covered earlier in this chapter appear to dominate in productive
ecosystems, where models predict that grazing selects for palatable, nutrient-rich plants
(i.e. tolerance strategy) (Grime 1977; Coley et al. 1985) which readily supply labile
substrates to soil as nutrient-rich litter and root exudates (Bardgett and Wardle 2003). In
contrast, negative effects of grazing on soil biota and nutrient cycling dominate in less-
productive situations, where models predict that grazing selects for unpalatable, slow-
growing plants (i.e. avoidance strategy) (Grime 1977; Grime 2001; Coley et al. 1985).
As highlighted earlier in this chapter, these unpalatable plants have traits that result in
poor-quality litter which decomposes slowly and therefore reduces nutrient availability
and plant growth (Bardgett and Wardle 2003). Moreover, selection for unpalatable
plants, and hence negative effects on soil nutrient cycling, are likely to be stronger with
grazing history (Bardgett et al. 2001b), which is consistent with the emphasis that is
placed on grazing history in modulating plant trait responses to grazing (Herms and
Mattson 1992; Díaz et al. 2006). Also, the above feedbacks resulting from herbivory
will further enforce the dominance of particular plant traits, thereby strengthening the
effects of herbivores on the ecosystem. For example, the selection of plant traits linked
to grazer tolerance in productive situations and consequent promotion of nutrient
cycling should further encourage plants with this growth strategy. In contrast, the
selection of plant traits linked to grazer avoidance in less-productive systems and
consequent slowing-down of nutrient cycling, would further enhance the success of
plants that exhibit an avoidance strategy (Bardgett and Wardle 2003).
A handful of studies have experimentally investigated the linkages between her-
bivory or foliage palatability, plant traits, and belowground processes. For example,
comparative studies across multiple plant species in temperate (Grime at al. 1996;
Cornelissen et al. 1999) and sub-Arctic (Cornelissen et al. 2004) communities have
found the palatability of foliage to herbivores and decomposability of plant litter to be
significantly correlated because both processes are governed by similar suites of
functional traits. Likewise, Wardle et al. (2002) used a broad range of plant species
collected from New Zealand forests to show that plant species that produced high-
quality litter that decomposed rapidly were also those that were disadvantaged by
selective browsing (i.e. more palatable), whereas those that produced poor-quality
litter were those that were advantaged by browsing (i.e. less palatable). Consequently,
it was concluded that the decomposability of litter and vegetation responses to
herbivory are governed by the same, or similar, suites of traits, notably the concen-
tration of secondary metabolites and structural carbohydrates in plant tissue. How-
ever, the relationship between foliage palatability and litter decomposability is not
universal, and Kurokawa and Nakashizuka (2008) found no evidence of such a
relationship among a large number of tropical rainforest tree species in Sarawak,
Borneo. With regard to the decomposer biota, little is known about the role of plant
traits in regulating the response of soil organisms to defoliation. However, Guitian
and Bardgett (2000) found that grass species varied in their allocation response to
defoliation, and that the greatest soil microbial response was detected in the species
that allocated most resources to roots when subjected to clipping. Further studies are
 4.4 Aboveground trophic cascades • 137

clearly needed in this area to determine how these responses relate to inter-specific
differences in plant traits, especially in the context of variation among grasses in
their relative investment of resources into growth (i.e. tolerance) and anti-herbivore
defence (avoidance). In this light, Massey et al. (2007) showed that 18 grass species
varied considerably in their investment in defence and growth rate, and that the two
attributes were negatively correlated. This suggests that there is likewise a spec-
trum of belowground responses to herbivory at the individual species level, which
relate to the balance of allocation of resources to growth (i.e. tolerance) and defence
(i.e. avoidance).
There is clearly much to be learned about plant trait responses to grazing and how
they link to belowground biota and the processes of decomposition and nutrient
cycling that they drive. However, the evidence presented here, albeit based on a
limited number of traits and studies, suggests that a conceptual framework for
investigating plant trait responses to herbivory could be extended to incorporate
belowground responses, and hence provide a basis for improved understanding the
consequences of herbivory for ecosystem function in different contexts. However,
as highlighted by Díaz et al. (2006), this requires more investigations of plant trait
responses to grazing that both follow a common framework (e.g. by using a
common list of traits) and are conducted across several contrasting locations.
Moreover, while there is much understood about how plant traits may drive above-
ground–belowground linkages and feedbacks (as discussed in Chapter 3), our
knowledge of how plant traits select for traits of soil organisms and vice versa is
lacking. Such information is required to develop an improved mechanistic under-
standing of herbivore effects on aboveground–belowground linkages and how these
linkages drive ecosystem processes.

4.4 Aboveground trophic cascades and consequences

for belowground properties
Aboveground herbivores are consumed by their predators, which are well known to
influence their densities and population dynamics. This can in turn lead to cascading
effects, or trophic cascades that affect the biomass, productivity, and composition of
the plant community. While there has been some historical debate about the import-
ance of trophic cascades in terrestrial ecosystems (e.g. Strong 1992; Polis 1994), and
there are many ecosystems for which they are probably unimportant, there is a
cumulating number of examples for which they have been shown to be of great
importance (Pace et al. 1999; Halaj and Wise 2001; Terborgh and Estes 2010). As
described so far in this chapter, herbivores can exert both positive and negative
effects on the functioning of the belowground subsystem through their influence on
individual plants and plant communities. It therefore follows that predators of
herbivores should reverse these effects, at least if they substantially reduce herbivore
densities and therefore the extent of herbivory in the ecosystem (Fig. 4.12). However,
despite widespread awareness of the importance of belowground trophic cascades for
138 • 4 Significance of aboveground consumers

PREDATORS
(CARNIVORES)

Foliar
herbivores

Plant community
Plant
structure
productivity

Litter quantity Rhizosphere

exudation Faecal
and quality
return

Decomposer
microflora
CARBON AND
NUTRIENT
Decomposer MINERALIZATION
fauna

Fig. 4.12 Schematic diagram of the mechanistic basis through which aboveground
carnivores can indirectly influence decomposer organisms and the ecosystem-level processes
that they perform. Adapted from Wardle et al. (2005).

soil processes and ecosystem functioning (see Chapter 2), and recent interest in how
predator diversity might influence ecosystem functioning (Duffy et al. 2007; Bruno
and Cardinale 2008), the issue of how aboveground trophic cascades affect the
functioning of the belowground subsystem has only recently attracted attention
(e.g. Feeley and Terborgh 2005; Wardle et al. 2005; Maron et al. 2006; Schmitz
2008a; Wardle 2010).
Predators of herbivores have been shown in some studies to potentially alter the
quality and quantity of resources entering the belowground subsystem; this in turn
has the potential to alter the soil food web and processes driven by the decomposer
subsystem. First, top predators can greatly alter the functional composition of the
vegetation by altering the levels of herbivory that the vegetation is subjected to. For
example, as will be discussed in Chapter 5, cougars (Puma concolor) and wolves
(Canis lupus) in North America are well known to reverse the negative effects of their
 4.4 Aboveground trophic cascades • 139

prey (cervids such as deer, elk, and moose (A. alces) on the forest understorey and
the growth of palatable deciduous plant species (Ripple and Betscha 2008; Creel
and Christianson 2009). This will in turn reverse the effects of cervids on the quality
of litter entering the decomposer subsystem (e.g. Pastor et al. 1993). Second,
predators of herbivores may reverse the effects that herbivores have on secondary
leaf chemistry, and therefore the quality of leaf litter that the plant subsequently
returns belowground. Evidence for this emerges from the study of Stamp and
Bowers (1996) who found that the induction of defence compounds (iridoid
glycosides) in Plantago lanceolata by invertebrate herbivores was reversed by
the predators of these herbivores. Third, predators can reverse the effects of
herbivores on the quantity of resources entering the belowground subsystem. For
example, Post et al. (1999) showed on Isle Royale, Michigan, USA, that predation
of moose by wolves reverses the adverse effect of moose on the radial growth of
Abies balsamea trees, and that, over time, radial growth tracks the population
dynamics of wolves. This would in turn reduce the quantity of resources that A.
balsamea inputs to the belowground subsystem. As an example of cascading effects
of predators at a whole ecosystem scale, Terborgh et al. (2001, 2006) used islands
created by a hydroelectric impoundment in Venezuela to highlight the indirect
impact of predator-induced trophic cascades on vegetation characteristics. Here,
small islands lack predators such as large snakes, raptors, jaguar (Panthera onca),
and puma (Puma concolor), and as such have hyper-abundant animals of lower
trophic status such as rodents, howler monkeys (Alouatta spp.), iguanas, and leaf-
cutter ants. The net result of this lack of predators is a substantial reduction in
seedlings and saplings of canopy tree species (Terborgh et al. 2006), and an
apparent shift to plant species that are less preferred by the herbivores and which
probably have poorer-quality litter (Feeley and Terborgh 2005).
Although top predators indirectly control the quantity and quality of plant-derived
materials entering soil, the consequences of this for the belowground subsystem have
been explicitly studied only recently. For example, Frank (2008) found that rates of
soil nitrogen mineralization were negatively influenced by the consumption of
ungulates by wolves (Canis lupus), and Feeley and Terborgh (2005) showed that
mammalian predators of other mammals and leaf-cutting ants reduced carbon-to-
nitrogen ratios in the soil. Further, Wardle et al. (2005) showed that predators of
aphids indirectly enhanced soil carbon concentrations, and Dunham (2008) showed
that insectivorous birds and mammals had important indirect influences on soil
phosphorus turnover. These predator-induced changes in soil chemical properties
are likely to be linked to changes in the composition of the soil biota, but few studies
have investigated whether aboveground trophic cascades instigated by aboveground
predators trickle through to the soil food web. However, in the study of Dunham
(2008), the exclusion of insectivorous birds and mammals was found to have indirect
positive effects on soil-associated invertebrate taxa known to be important for driving
soil processes (Fig. 4.13). Further, in a manipulative glasshouse experiment, Wardle
et al. (2005) showed that aboveground predators of aphids (lacewings and a ladybird
beetles) induced a trophic cascade that altered plant species composition and thereby
140 • 4 Significance of aboveground consumers

(a)

140 Control
300
Macro-invertebrate density (per m2)

Exclosure
120
Rainfall 250
100

Rainfall (mm)
200
80
150
60
100
40

20 50

0 0
Mar Apr May Jun Jul Aug Sep Oct Nov

(b)
60 Control
* Exclosure
**
50
**

40
Abundance

30

20

10

0
Micro- Macro- Earthworms
invertebrates invertebrates

Fig. 4.13 Abundance of soil invertebrates in plots with and without exclusion of top above-
ground predators (mammalian and avian insectivores) in tropical rainforest in Coté d’Ivorie.
(a) Total macroinvertebrate density in exclosure and control plots over an 8 month period;
(b) total abundance of invertebrate groups in exclosure and control plots summed over an 8 month
period; *, ** indicates statistical significance at P ¼ 0.05 and 0.01 respectively. Error bars are
SE. From Dunham (2008), with permission from Wiley-Blackwell.

promoted the primary consumers (microflora) and tertiary consumers (top predatory
nematodes) of the soil food web. The aboveground predators also sometimes indir-
ectly altered microbial community structure, promoting bacteria at the expense of
fungi, and reduced the diversity of herbivorous nematodes. In contrast, in an experi-
mental study involving an understorey forest shrub, Dyer and Letourneau (2003)
 4.5 Spatial movement of resources • 141

showed that species diversity within each of three consumer trophic levels in a
decomposer food web was unaffected by manipulation of a top predatory beetle
that feeds upon herbivorous and possibly detritivorous insects; diversity within each
trophic level was instead driven mainly by the manipulation of basal resources.
Collectively, these studies highlight the multitrophic linkages that can exist between
aboveground and belowground food webs, and which may involve multiple trophic
levels both above and belowground.
As discussed for foliar herbivores, aboveground predators of herbivores can vary
greatly in their effects on the belowground subsystem. This arises not just through
predators reversing the effects of herbivores (which themselves can have positive or
negative effects), but also through the influence of predator identity in its own right.
First, different predators may differentially affect the population dynamics of their
herbivorous prey, and thus the temporal pattern of plant material addition to the
belowground subsystem. For example, Wardle et al. (2005) found that two different
predators of aphids differed greatly in their effects on the timing of peaks in aphid
populations, and therefore their effects on both the plant and soil community. Second,
different predator species differ greatly in prey specificity. It is expected that indirect
effects of aboveground predators on the belowground subsystem are greatest when they
are relatively specific, and when they feed on herbivore taxa that are themselves major
drivers of the ecosystem. These effects may be less strong for generalist predators in
reticulate food webs (Polis 1994) or for aboveground predators that feed on both
herbivores and decomposers (Scheu 2001). Third, differences in behaviour or hunting
mode between different predator species may influence herbivore feeding pattern, and
therefore the plant community and belowground properties (Schmitz et al. 2004). This
idea has been little explored, although Schmitz (2008b) found that two grasshopper-
feeding spider species with different feeding modes, one being an active hunter and the
other being a sit-and-wait ambush predator, exerted opposing effects on plant diversity,
net aboveground primary productivity and rates of soil nitrogen mineralization in
grassland. These effects were attributed to different responses to the two different
predators by their grasshopper prey, the dominant herbivore species in this grassland
system, although whether these predators had opposing effects relative to predator-free
conditions is not known. Finally, some of the strongest belowground effects of above-
ground trophic cascades have involved aboveground consumers being subjected to
predation pressures to which they have not evolved, for example through invasions by
novel predators, or through hunting by humans colonizing new land masses; trophic
cascades of this type will be explored in Chapter 5.

4.5 Spatial movement of resources by

consumer organisms
The preceding sections illustrate how aboveground consumers modulate the func-
tioning of terrestrial ecosystems through a variety of mechanisms. Through their
movements and foraging behaviour, consumer organisms can also transfer resources
142 • 4 Significance of aboveground consumers

both within and between terrestrial ecosystems, largely through their faeces and
carcasses, with potentially major consequences for spatial patterns of nutrient
cycling and vegetation. Moreover, terrestrial ecosystems are also affected by both
terrestrial and aquatic consumers that are capable of transferring resources from
aquatic to terrestrial habitats, with potentially major consequences for terrestrial
ecosystems both aboveground and belowground. Here, we discuss the conse-
quences of these types of consumer-mediated resource subsidies for terrestrial
ecosystems. First we explore the consequences for both the aboveground and
belowground subsystem of consumer-mediated resource distribution within and
between terrestrial ecosystems, and second we examine the consequences of
resource transfers from aquatic to terrestrial ecosystems by aquatic and terrestrial
consumers.

4.5.1 Resource transfers across land

Movement of mammalian herbivores during foraging is driven both by their behav-
ioural repertoire and by livestock management, and operates at a range of temporal
and spatial scales (Bailey and Provenza 2008; Boone et al. 2008). For example, wild
herbivores may move up and down elevation zones to take advantage of temporal
variation in plant phenology and forage quality, or they might migrate from one
region to another due to forage or water shortages, or changes in precipitation patterns
(Bailey and Provenza 2008). At finer scales, wild herbivores may move relatively
short distances (metres to kilometres) to select feeding sites where forage is more
abundant or nutritious, or to carry out non-foraging activities such as resting and
ruminating (Bailey and Provenza 2008). Likewise, in livestock systems, herbivores
are moved from field to field to maximize forage use, and herders move their animals
to varying degrees in response to extreme climatic conditions or to allow them to cope
with seasonal changes in forage supply (Boone et al. 2008). For example, in the
Mongolian steppe, herders can move livestock over distances ranging from 10 km
several times a year, to over 300 km between the mountains and lowlands, to make
the best use of forage supply across a range of habitats. Meanwhile, in mountainous
regions, herders move their livestock from sheltered valleys to higher elevations
during the summer months to make use of snow-free mountain meadows (Boone
et al. 2008). Given the potential for herbivores to modulate soil nutrient cycling and
vegetation dynamics (as discussed so far in this chapter) and also to transfer resources
from one site to another in their faeces and bodies, such herbivore movements will
inevitably have important consequences for spatial patterns of nutrient cycling and
vegetation.
Despite the tremendous research effort that has gone into understanding the
behavioural mechanisms that result in grazing distribution patterns (reviewed by
Bailey and Provenza 2008), comparatively little is known about the consequences
of herbivore movement for nutrient transfers within and across ecosystems. More-
over, most of what is known is from agricultural situations, where several studies
have shown that livestock promotes the patchy return of nutrients through using
 4.5 Spatial movement of resources • 143

different parts of their habitat for feeding and for excretion. For example, Edwards
and Hollis (1982) found that grazing by horses on pastures in the New Forest in
southern England created a pattern of latrine and grazing areas, with generally
higher concentrations of soil nutrients and greater plant biomass in the latrine areas.
This is similar to the previously mentioned example of Willot et al. (2000), who
found that although rabbits deposit dung throughout their range, dung deposition is
greatest in places where they congregate, and a large amount of dung is deposited
in a small number of latrines. Likewise, although cattle tend to deposit their dung
haphazardly in level pastures (White et al. 2001), a large proportion of this dung is
often input to areas that they use for resting and ruminating. Consequently, soil
nutrients become concentrated in relatively small areas where the animals spend a
large proportion of their time (Syers et al. 1980; Afzal and Adams 1992; Kohler
et al. 2006).
Several studies have also explored the consequences of redistribution of nutrients
through faeces for nutrient budgets and pasture production. For example, in a study of
Brachiaria pastures in Brazil, Boddey et al. (2004) found that increasing cattle
stocking rates caused a decline in pasture quality because more nitrogen was depos-
ited in the form of urine and faeces, leading to substantial gaseous and leaching losses
of nitrogen. Moreover, much of this N was deposited in rest areas and around
drinking troughs where the vegetation was too trampled to derive much benefit
from it, while the availability of nitrogen in other areas was correspondingly reduced
(Boddey et al. 2004). Similarly, in a study of mountain pastures in the Swiss Alps,
Jewell et al. (2007) found that cattle redistribute substantial amounts of phosphorus
by feeding and defecating in different places. They found that cattle dropped most of
their dung in relatively small areas where they gathered for ruminating and resting,
and, as a result, a few small patches had accumulated high amounts of phosphorus (in
excess of 50 kg P ha1 year1), while much larger areas of pasture had become
depleted. They concluded that by concentrating nutrients in small areas, cattle
promote nutrient loss from mountain pastures and thus cause a gradual decline in
their productivity. However, they also note that the significance of this type of
nutrient redistribution for long-term pasture production will depend upon factors
such as the stability of the spatial pattern caused by cattle and the magnitude of the
phosphorus depletion relative to other ecosystem inputs and outputs.
Relatively few studies have explored the influence of herbivores on nutrient
translocation and spatial distribution of soil nutrients in natural ecosystems,
although similar mechanisms as described above are likely to be at play, albeit
over larger spatial scales. For example, Schütz et al. (2006) examined the role of
red deer in the redistribution of phosphorus (the primary limiting nutrient) in a
subalpine grassland ecosystem in the Swiss Alps. They compared phosphorus
removal by grazing of aboveground plant biomass with phosphorus input due to
the deposition of faeces, across an extensive sampling gird that covered the entire
ecosystem. Using this approach, they found that the proportion of heavily grazed
short-grass vegetation (dominated by Festuca rubra and Briza media) in the
landscape increased with increasing soil phosphorus content, indicating that red
144 • 4 Significance of aboveground consumers

deer preferably grazed patches that were more phosphorus-rich. They also found
that rates of phosphorus removal by grazing in the phosphorus-rich areas was
greater than from phosphorus-poor areas, and that this enhanced loss was in excess
of the increase of phosphorus input due to greater faecal deposition, leading to an
average annual net phosphorus loss. This net loss, was, however, very low (i.e.
0.083 kg ha1) and it was estimated that it would take 1660 years for the soil
phosphorus pool in the most phosphorus-rich parts of the ecosystem to be depleted
to the levels observed in the phosphorus-poor parts. They also noted that the yearly
net phosphorus loss caused by grazing was comparable to that reported for vege-
tation communities grazed by elk in the Rocky Mountain National Park, USA
(Schoenecker et al. 2002), indicating that phosphorus translocation by herbivores in
these types of grazing systems may impact on the spatial dynamics of vegetation
only in the long-term.
While the above example concerns soil phosphorus, there is also evidence that
large herbivores in natural grassland influence the spatial distribution of soil
nitrogen and rates of nitrogen mineralization across a wide range of spatial scales.
For example, McNaughton et al. (1997b) found that free-ranging resident grazers,
principally Thomson’s (Gazella thomsoni) and Grant’s (Gazella granti) gazelles,
topi (Damaliscus korrigum), and kongoni (Alcelaphus buselaphus), enhance rates
of nitrogen mineralization and sodium availability in areas where they preferen-
tially graze, and thus contribute to the spatial heterogeneity of soil fertility at the
landscape scale. Also, Augustine and Frank (2001) found that native migratory
ungulates, namely elk, bison, and pronghorn antelope, influenced the spatial distri-
bution of soil nitrogen and rates of nitrogen mineralization at a range of spatial
scales in grasslands of Yellowstone National Park, USA. Through geostatistical
analyses of soils collected inside and outside long-term fenced exclosures, they
found that grazers altered the spatial distribution of soil nitrogen properties at all
scales ranging from individual plants (<10 cm), to whole plant communities
(30 m), to topographically variable landscapes. Finer-scale heterogeneity was
attributed to the promotion of local plant species diversity, variation in plant
turnover by grazers, and possibly the patchy return of urine and dung. In contrast,
landscape-scale variability, which was significantly enhanced by grazers, was
attributed to variation in grazing intensity, bedding-site selection, and dunging
across the topographically variable site. Indeed, it is well known that elk respond
to heterogeneity in forage production by concentrating in areas of high productivity
at any one time (Frank and McNaughton 1992) and by landscape-scale selection of
winter grazing locations based on elevation and grassland type (Pearson et al.
1995). Overall, these results were taken to demonstrate that, in addition to the
effects of topography and vegetation on spatial patterning of soil nutrients, biotic
components of ecosystems such as large herbivores not only respond to resource
heterogeneity, but also play a significant role in contributing to it.
A further mechanism by which herbivores can enhance spatial heterogeneity in
nutrient cycling and vegetation at the landscape scale is through their carcasses,
which cause concentrated pulses of nutrients into the soil. This mechanism is poorly
 4.5 Spatial movement of resources • 145

explored, but some studies clearly point to significant and lasting effects of carcasses
in terrestrial ecosystems. For example, Towne (2000) studied the effects of ungulate
carcasses in tallgrass prairie in Kansas, USA, and found that they created hotspots of
soil fertility and plant production, thereby increasing community heterogeneity.
However, as emphasized by Towne (2000), the significance of ungulate carcasses
as contributors to grassland vegetation dynamics and nutrient cycling becomes
especially significant when considered from a historical perspective: episodic disas-
ters such as severe droughts, harsh winters, or endemic disease can produce high rates
of herbivore mortality, and hence such historical events have enriched grasslands for
eons (Towne 2000). In another study, Bump et al. (2009c) showed that carcasses of
white-tailed deer (Odocoileus virginianus) created biogeochemical hotspots that
contributed to resource heterogeneity and shifting tree competitive interactions in
northern hardwood forest in the Upper Peninsula of Michigan, USA. Moreover,
Bump et al. (2009a) showed that heterogeneity in soil nutrients and plant nutrient
content caused by carcasses, in this case of moose (A. alces) in boreal forest of Isle
Royale National Park, Michigan, USA, was modulated by wolves (C. lupus).
Through their predatory behaviour, wolves influenced the spatial distribution
of moose carcasses, which in turn determined spatial patterns of soil nutrients,
microbial communities, and plant tissue quality (Fig. 4.14). Meanwhile, Parmenter
and MacMahon (2009) studied the effects of carcass decomposition of a wide range
of vertebrates (including mammals, two birds, a snake species, and one frog species)
on soil nutrients in semiarid shrub-steppe in Wyoming, USA. Regardless of source,
they found that carrion-decomposition processes enriched soils in nitrogen in the
vicinity of the carcass, causing localized changes in the plant community. Although
this contributed minimally to the total nitrogen budget of the ecosystem, it was argued
that vertebrate carcasses have an impact on soil nutrient status and turnover at the
local patch-scale level, thereby contributing to community heterogeneity.
Finally, it is important to note that carcasses of invertebrates can also significantly
impact on terrestrial ecosystems. This is best illustrated by the study of Yang (2004),
who examined the ecological effects of resource pulses resulting from periodic
deposition of carcasses of cicadas of the genus Magicicada. These insects, which
can be the most abundant herbivore in North American deciduous forests, spend most
of their lives belowground feeding on xylem in tree roots, but every 17 years they
emerge in vast numbers, mate, lay eggs, and die. Yang (2004) simulated a cicada
emergence event by applying cicada carcasses to the forest floor, and found this to
stimulate the biomass of soil bacteria and fungi, soil inorganic nitrogen availability,
and hence the nitrogen content and seed mass of an understorey plant, the American
bellflower (Campanulastrum americanum) (Fig. 4.15). Given that the spatial distri-
bution of cicadas is highly variable and dynamic at the landscape scale, Yang (2004)
argued that the patchiness of cicada distributions may contribute to spatial and
temporal heterogeneity in resource pulse effects in forest ecosystems. Also, as high-
lighted by Yang (2004), while these findings result from the unusual life history of a
single insect genus, they illustrate a more general potential consequence of resource
pulses for aboveground and belowground subsystems.
146 • 4 Significance of aboveground consumers

(a)

500
Carcass
*
Inorganic N (mg/kg)
400 Control

300
*

200

100

0
(b)
250
*
200
* *
P (mg/kg)

150

*
100

50

0
(c)
900
*
750

600 *
K (mg/kg)

450

300

150

0
0 5 10 15 20 25 30 35 40
Months post-mortality

Fig. 4.14 Impact of carcasses of moose (Alces alces) killed by wolves (Canis lupus) on soil
nutrients in the boreal forest of Isle Royale National Park, Michigan, USA. Data show soil
concentrations of (a) inorganic nitrogen (nitrate þ ammonium), (b) phosphorus, and
(c) potassium in soils from wolf-killed moose carcass sites (solid circles) and paired control
sites (open circles) at 4, 16, 28, and 40 months post-mortem. Asterisks indicate significant
(P < 0.05) differences between carcass and control sites at each postmortem sampling time.
Error bars show means+SE (some are too small to be seen). Note the different y-axis scales.
From Bump et al. (2009a), with permission from the Ecological Society of America.
 4.5 Spatial movement of resources • 147

(b)

(a)
(c)

17 years ~ 3 months

(d)
N

N N
N N
N
N
N N
N

Fig. 4.15 Schematic of the belowground and aboveground effects of a 17-year pulse of
nitrogen from cicada carcasses: (a) for 17 years, cicada nymphs feed on tree xylem, slowly
incorporating belowground nitrogen (N) absorbed by the tree’s roots; (b) upon emergence,
adult cicadas mate and lay eggs within a several-week period, and then die and drop to the
forest floor; (c) the accumulated nitrogen in their carcasses is released after a burst of activity by
microbial decomposers; and (d) this spike of available soil nitrogen leads to increased nitrogen
content and seed size of the American bellflower (Campanulastrum americanum), an under-
storey plant. From Ostfeld and Keesing (2004) and derived from Yang (2004), with permission
from the American Association for the Advancement of Science.

4.5.2 Resource transfers from aquatic to terrestrial ecosystems

Most terrestrial ecosystems occur in the proximity of aquatic ecosystems, such as
oceans, lakes, rivers, and streams. Aquatic and terrestrial communities do not func-
tion independently of one another, and there are numerous examples of interactions
between these two communities, especially at their interface. As such, terrestrial
ecosystems are affected not just by terrestrial consumers that derive their energy from
terrestrial plants, as discussed so far in this chapter, but also by both terrestrial and
aquatic consumers that derive at least part of their resources from the aquatic
environment. It is well known, for example, that many riparian terrestrial predators
can obtain a large proportion of their nutrition from aquatic prey (Sabo and Power
2002; Ballinger and Lake 2006), and that emerging aquatic insects which spend their
larval phase in the water can have major effects on terrestrial communities during
their adult phase (Knight et al. 2005; Gratton and Vander Zanden 2009). Both aquatic
148 • 4 Significance of aboveground consumers

and terrestrial consumers are capable of transferring resources from aquatic to

terrestrial habitats, with potentially major consequences for terrestrial ecosystems
both aboveground and belowground. We now discuss the consequences of this type
of consumer-mediated resource subsidy for the functioning of terrestrial ecosystems.
Many of the strongest and best documented examples of aquatic to terrestrial
resource transfer involves seabird activity on coastal and island ecosystems (Polis
et al. 1997; Anderson et al. 2008). Here, seabirds feed on aquatic organisms (mainly
fish) in the ocean, and deposit them as guano on nearby terrestrial ecosystems. These
inputs can represent the main source of nutrient inputs for unproductive terrestrial
ecosystems adjacent to productive marine ecosystems (Polis and Hurd 1996). For
example, in coastal ecosystems in Antarctica, plant communities are very unproduct-
ive and dominated by lichens and mosses, and they therefore input very little organic
matter to the soil. Here, nesting Adélie penguins transfer large quantities of nutrients
and organic matter from the ocean to their nesting colonies, leading to the formation
of ornithogenic soils that can contain up to 100 times the density of soil bacteria and
microbial biomass that occurs in nearby non-ornithogenic soils (Ramsay 1983; Roser
et al. 1993). Another system which has been extensively studied involves desert
islands in the Gulf of California, some of which support large colonies of nesting
seabirds and others of which do not (Polis and Hurd 1996; Wait et al. 2005; Anderson
et al. 2008). Those islands which contain seabird colonies, and therefore receive high
inputs of ocean-derived resources, have concentrations of soil nutrients that are
several times greater than those that lack seabirds (Anderson and Polis 1999). This
enhanced nutrient input has important bottom-up effects on a range of arthropod taxa
and causes a multiple-fold increase in tenebrionid beetles that serve as the main
macrofaunal detritivore on the islands (Sanchez-Piñero and Polis 2000). Subsequent
studies have also pointed to important positive effects of seabirds on soil nutrient
availability on more productive island and coastal systems, for example in New
Zealand (Mulder and Keall 2001; Fukami et al. 2006), the Aleutian Islands in Alaska
(Maron et al. 2006), the north-eastern USA (Ellis et al. 2006), and the Great Barrier
Reef in Australia (Schmidt et al. 2004). Also, on offshore islands in northern New
Zealand, high seabird densities have been shown to greatly enhance densities of a
range of belowground groups of soil invertebrates (Towns et al. 2009) and indirectly
alter rates of plant litter decomposition (Fukami et al. 2006). Likewise, nitrogen
enrichment from seabird colonies on the Isle of May, in the Firth of Forth, east
Scotland, was found to stimulate microbial biomass and abundance of nematodes in
soil, and increase the abundance of bacteria relative to fungi, although no effects on
soil functioning (e.g. rates of nitrogen mineralization and decomposition) were
detected (Wright et al. 2010).
Nutrient transfer by seabirds from ocean to land in turn has important conse-
quences aboveground for plant nutrient acquisition and growth (Ellis 2005). For
example, plants in soils associated with seabird colonies have been shown to grow
much more rapidly (Fukami et al. 2006), and contain greater levels of foliar nutrients
(Maron et al. 2006; Mulder et al. 2009) than plants growing in soils without seabird
colonies. Plants in seabird colonies may also produce litter that decomposes and
 4.5 Spatial movement of resources • 149

(a) (b)

Fig. 4.16 Photographs of (a) arid vegetated island with seabird nutrient inputs and
(b) vegetation-poor island without seabird nutrient inputs derived from the ocean in the Gulf
of California (Wait et al. 2005; Anderson et al. 2008). Images by A. Wait.

releases nutrients more rapidly (Wardle et al. 2009b), and foliage that is more
palatable to foliar herbivores (Mulder and Keall 2001). These positive effects of
seabird colonies on plant growth and nutrition are particularly pronounced for ruderal
or annual plant species (Anderson and Polis 1999; Ellis 2005) (Fig. 4.16). Seabird
colonies can also exert important negative effects on plant seedling recruitment,
growth, and biomass production, largely through increased physical disturbances
(Maesako 1999). For example, while high seabird densities on forested oceanic
islands in north-east New Zealand lead to greater nutrient uptake by plants, these
effects are offset by the adverse effects of soil perturbation associated with burrowing
during nesting, leading to both lower densities of tree seedlings (Fukami et al. 2006)
and a large net reduction in aboveground standing biomass (Wardle et al. 2007). As
such, while high seabird densities alleviate nutrient limitation of plants, they also
increase limitation of plants by physical disturbance and tissue damage, although the
relative importance of these two opposing forces has been seldom explored. The
combined effects of less nutrient stress and greater disturbance has important conse-
quences for plant community composition, and there is a common trend for seabird
activity to favour domination by short-lived and fast-growing ruderal species at the
expense of longer-lived and slow-growing species (Ellis 2005). As discussed in
Chapter 3, these types of plant community-level shifts can potentially feedback to
the belowground community through greater quality of plant-derived resources,
although this has yet to be investigated for seabird-dominated ecosystems.
Resources transported by consumers from fresh water to land can also serve as
important ecosystem drivers. For example, moose in Isle Royale, USA, feed on
aquatic macrophytes and deposit them as faecal material in nearby riparian forests,
thereby increasing soil nitrogen availability (Bump et al. 2009b). This stimulation
may help counter the negative effects of moose on nitrogen availability through other
mechanisms described in this chapter (Pastor et al. 1993). Another example involves
fertilization of riparian forests by dead salmon (Oncorhynchus spp.) in Alaska and
150 • 4 Significance of aboveground consumers

Fig. 4.17 Cycling of salmon-derived nitrogen and effects on river and riparian ecosystems:
(a) spawning salmon transport nitrogen upstream; (b) bears (Ursus spp.) and other piscivores
consume salmon; (c) bears disseminate salmon-enriched wastes and partially eaten salmon
carcasses in the riparian forest; (d) terrestrial and aquatic insects colonize salmon carcasses,
enhancing decomposition and nitrogen diffusion; (e) dissolved nitrogen downwells beneath the
riparian forest and is taken up by tree roots; (f) salmon-derived nitrogen enhances foliar
nitrogen and growth rates of riparian trees; (g) riparian trees provide shade, bank stabilization,
and coarse woody debris, enhancing the quality of instream habitat for salmonid fishes;
(h) coarse woody debris retains post-spawn salmon carcasses in streams, further enhancing
nitrogen availability; and (i) increased foliar nitrogen enhances palatability of riparian plants,
potentially altering patterns of browsing, which in turn affects patterns of riparian productivity
and species composition. Redrawn from Helfield and Naimann (2006) by D.W. Colquhoun.

British Colombia (Helfield and Naiman 2006) (Fig. 4.17). Here, bears (Ursus spp.)
capture salmon from rivers during spawning, and can carry over 70% of captured
salmon into the forest to avoid other bear (Quinn et al. 2009). A large proportion of
the captured salmon biomass is never consumed (Gende et al. 2001; Holtgrieve et al.
2009). Therefore, dead salmon serve as an important nitrogen input into these
forests, accounting for up to 24% of ecosystem nitrogen input, which is greater
than that derived from nitrogen fixation by alders (Helfield and Naiman 2006).
Further, this nitrogen is highly labile, and fertilization by dead salmon can therefore
cause substantial local increases in soil mineral nitrogen concentrations (Gende et al.
2007), leading to increased nitrogen uptake by soil microbes and plants (Helfield and
Naiman 2002, 2006; Wilkinson et al. 2005) and enrichment of d15N in litter-dwelling
 4.5 Spatial movement of resources • 151

invertebrates (Hocking and Reimchen 2002). It has been proposed that these
responses in turn cause an increase in the nitrogen content and hence palatability
of plant foliage, thereby potentially altering patterns of browsing by herbivores
(Helfield and Naiman 2006) (Fig. 4.17).
Aquatic-derived invertebrates also have the potential to serve as terrestrial ecosys-
tem drivers. Indeed, a handful of studies have shown that insects that spend their
developmental stages in rivers (Sabo and Power 2002; Ballinger and Lake 2006) and
lakes (Hyodo and Wardle 2009; Jonsson and Wardle 2009) may serve as a major
source of prey for terrestrial predators when they emerge on land as adults. Little is
known about the consequences of aquatic-derived invertebrates for the functioning of
terrestrial ecosystems either above or below ground, although a recent study per-
formed in lakes (including Lake Myvatn) in Iceland offers some insights (Gratton
et al. 2008). Here, very high densities of midges (chironomid flies) can emerge from
the lakes, with numbers varying greatly among years (Ives et al. 2008). Midges often
die on land, and their input of nitrogen to the surrounding terrestrial ecosystem is
probably in the order of 200 kg N ha1 year1 (data in Gratton et al. 2008), which
could represent a major fertilization effect, with important consequences for both
aboveground and belowground properties (Gratton and Vander Zanden 2009). Stable
isotope analyses have shown that this input of midges probably serves as an important
resource for key decomposer groups such as collembolans and soil-associated pred-
ators, including opilionids and lycosid spiders (Gratton et al. 2008). It is not known
how widespread this type of effect is, although recent evidence from stable isotope
studies suggests that dead chironomids could also fertilize island ecosystems in lakes
in northern Sweden (Hyodo and Wardle 2009).
Studies of the impact of aquatic organisms on the structure and function of adjacent
terrestrial ecosystems are still in their infancy, with most studies to date being focused
on the transfer of dead marine organisms to land by either seabirds or bears. As such, it
is difficult to draw generalizations about how and when aquatic to terrestrial inputs are
important. However, two factors may influence the extent to which terrestrial ecosys-
tems are affected by inputs from aquatic systems. First, it is expected that terrestrial
ecosystems may benefit most from aquatic inputs when the terrestrial system is much
less productive than the aquatic one (Polis and Hurd 1996). However, there is
evidence that aquatic resource subsidies can exert important effects on terrestrial
communities even when the terrestrial and adjacent communities are of comparable
productivity (Paetzold et al. 2008). Second, it is unclear as to whether these effects are
restricted only to terrestrial ecosystems very close to the shore or whether they can
extend some distance inland. For example, in the abovementioned case of midges
from Icelandic lakes, while the highest density of midges occurs at the lake edge, a
high density nevertheless still occurs at 150 m from the shore (Gratton et al. 2008).
Also, the transport of marine-derived nutrients by seabirds can occur much further
from the coast, given that seabirds in New Zealand may nest 50 km or more inland
(Worthy and Holdaway 2002). Much remains to be learned about whether large
effects of aquatic subsidies on terrestrial ecosystems represent a small collection of
special cases for specific types of ecosystems, or are more widely spread.
152 • 4 Significance of aboveground consumers

4.6 Aboveground consumers, carbon dynamics,

and global change
As discussed in Chapters 2 and 3, the effects of global change phenomena on
belowground communities and the processes that they drive operate via both direct
and indirect mechanisms, with often far-reaching consequences for ecosystem-level
properties and carbon-cycle feedbacks at regional and global scales. Indeed, as we
argue in Chapter 3, an understanding of the effects of global change phenomena on
terrestrial ecosystems and feedbacks, and also their potential mitigation, requires
explicit consideration of linkages between aboveground and belowground subsys-
tems. Given that herbivores can strongly modify these linkages, and that herbivore
behaviour and performance may be affected by global change both directly and
indirectly (i.e. via shifts in vegetation composition), it follows that herbivores should
act as key modulators of global change impacts on the functioning of terrestrial
ecosystems. Here, we illustrate this using soil carbon dynamics and climate change as
examples. We first examine how herbivores can modulate terrestrial ecosystem
carbon cycling, with potential consequences for carbon-cycle feedbacks, and then
consider how global change-induced shifts in vegetation composition could affect
herbivore populations with consequences for ecosystem functioning. We emphasize
that very little is known about these two issues; indeed, as noted recently by Gough
et al. (2007), most studies that have examined responses of vegetation and
soil properties to climate change have not explicitly considered interactions with
herbivores.
A considerable amount of research effort has gone into understanding how herbi-
vores influence soil biotic interactions and the functioning of terrestrial ecosystems.
As discussed so far in this chapter, most of this of this work has focused on the
cycling of plant growth-limiting nutrients (i.e. nitrogen and phosphorus) and plant
productivity. However, the same pathways by which herbivores impact on soil biotic
interactions and nutrient cycling will also influence soil carbon dynamics, and
potentially the amount of carbon that is stored in and lost from soil. Although a
growing number of studies have evaluated the effects of domestic livestock grazing
on grassland soil carbon stores (e.g. Schuman et al. 1999; Han et al. 2008; Gollusccio
et al. 2009), our understanding of how herbivores influence on ecosystem-scale
carbon stores and fluxes in natural ecosystems is limited. Further, only a handful of
studies have considered the role of herbivores in regulating soil biotic interactions
and carbon fluxes relative to climate change. We consider here some of what is
known about the role of herbivores in regulating soil carbon stores and fluxes to the
atmosphere in managed and natural ecosystems, and how such activities might
contribute to climate change via carbon-cycle feedbacks.
As outlined in Chapter 2, the amount of carbon stored in soil, and hence the
potential for soils to act as carbon sinks, is determined by the balance between the
input of carbon to soil via primary productivity (dead leaves, roots, and exudates)
and its loss via heterotrophic and autotrophic respiration (De Deyn et al. 2008).
Although abiotic factors (especially temperature and moisture) act as primary
 4.6 Aboveground consumers and global change • 153

determinants of these components of soil carbon flux, they are also strongly
regulated by aboveground consumers, as already outlined in this Chapter
(Fig. 4.18). In particular, herbivores can regulate the amount and quality of organic
matter entering soil as plant litter (shoot and roots) and as root exudates, and the
rate of decomposition of plant-derived organic matter by heterotrophic soil organ-
isms. Given the wide range of mechanisms by which herbivores can influence soil
carbon dynamics, it is unsurprising that the effects of grazing on soil carbon stores
and fluxes are highly variable. For instance, Milchunas and Lauenroth (1993)
carried out a review of 34 studies involving grazed and ungrazed sites around the
world and found that 40% of them reported a decrease and 60% an increase in soil
carbon stocks as a result of grazing exclusion. Consistent with this variability, more
recent studies of grasslands likewise report variable responses of soil carbon
content to livestock grazing, with increases (e.g. Schuman et al. 1999; Reeder
and Schuman et al. 2002), decreases (e.g. Frank et al. 1995; Bardgett et al. 2001b;
Han et al. 2008; Golluscio et al. 2009; He et al. 2009), and neutral effects (Shrestha
and Stahl 2008) being reported, even within the same study (Piñeiro et al. 2009).
Few studies have attempted to explain such differences in the response of soil
carbon storage to grazing. However, these differences have been attributed in part to

CO2

Aboveground
Litter Plants
herbivores and
predators
Exudates
Animal wastes

Soil C

Nutrients
(nitrogen and phosphorus)
Microbes

DOC

Soil faunal community

& diversity

Fig. 4.18 Schematic diagram showing the various routes by which aboveground consumers
influence carbon fluxes in terrestrial ecosystems. Solid lines represent inputs of carbon the soil
system, for instance from plant litter, root exudates, and animal wastes. Thick dashed lines
represent outputs of carbon in the form of dissolved organic carbon (DOC) and carbon dioxide
(CO2). Fine dashed lines represent a feedback to plant production and carbon input via altered
nutrient availability.
154 • 4 Significance of aboveground consumers

variation in soil physical properties (e.g. soil texture and depth), depth of soil
sampling, and responsiveness of the plant community to grazing (which in turn
determines the amount and quality of carbon allocated belowground) (Schuman
et al. 1999; Welker et al. 2004; Piñeiro et al. 2009). For instance, it has been proposed
that grazing can enhance soil carbon in situations where root biomass, and hence the
allocation of carbon belowground, is enhanced (Schuman et al. 1999; Piñeiro et al.
2009), or when declines in aboveground plant inputs to the soil are offset by manure
inputs (Conant et al. 2001). In contrast, declines in soil carbon are likely when heavy
grazing reduces plant biomass and the input of carbon to soil (Han et al. 2008; Pei
et al. 2008), or when grazing selects for palatable, nutrient-rich plants which readily
supply labile substrates to soil as nutrient-rich litter and root exudates. As discussed
earlier in this chapter, such labile substrates, as well as dung and urine, promote the
activity of decomposer organisms and bacterial-based energy channels, and hence
carbon loss from soil (Bardgett and Wardle 2003).
This latter idea, which is broadly consistent with the trait-based framework
discussed in section 4.3 and the acceleration/deceleration hypothesis presented in
Figure 4.2, was recently tested by Klumpp et al. (2007, 2009). These authors set
up a series of grassland monoliths which were subjected to simulated high and
low grazing pressure for 14 years, and found that monoliths exposed to low
grazing pressure were characterized by slow-growing, high-stature plant species,
fungal-dominated soil communities, and greater soil carbon content. In contrast,
monoliths exposed to high grazing were dominated by small-stature, fast-growing
plant species, bacterial-dominated soil communities, higher aboveground plant
productivity, and lower soil carbon storage (Klumpp et al. 2007). Further explor-
ation of the mechanistic basis for these trends revealed that high grazing pressure
caused a decline in root biomass and proliferation of soil bacteria, and an associated
acceleration in the decomposition of old particulate organic carbon in soil, leading
to a reduction in soil carbon storage (Klumpp et al. 2009) (Fig. 4.19). Collectively,
these findings indicate that heavy grazing of productive grasslands can promote
‘fast’-cycling microbial communities in soil, thereby accelerating decomposition
and carbon loss from soil. In contrast, situations where grazing selects for unpal-
atable, slow-growing plants that produce low-quality litter which decomposes
slowly, or where it promotes belowground allocation to roots, should lead to
enhanced soil carbon storage (Schuman et al. 1999; Welker et al. 2004; Piñeiro
et al. 2009). However, in making these conclusions we stress that there is much to
be learned about the ways that grazing influences soil carbon storage, and, as
highlighted above, many mechanisms are at play, suggesting that responses may
vary greatly among ecosystems.
The above studies all refer to soil carbon stocks, but the main challenges that
ecologists face in the context of global warming include quantifying the rates at
which ecosystems exchange carbon dioxide with the atmosphere, and determining
how these rates are controlled by abiotic, biotic, and management factors (Wohlfahrt
et al. 2008). A number of studies have examined how grazing influences soil respir-
ation (i.e. evolution of carbon dioxide from soil) in the field, and have reported
 4.6 Aboveground consumers and global change • 155

Grazing pressure

AVOIDANCE STRATEGY TOLERANCE STRATEGY

Slow-growing Fast-growing
Unpalatable Palatable
Low litter quality High litter quality

Fungal-dominated Bacterial-dominated
microbial communities microbial communities

Deceleration of
Accelerated rates of
decomposition and
decomposition and
soil carbon
soil carbon loss
accumulation

Fig. 4.19 Schematic diagram showing how shifts in vegetation and soil microbial community
composition influence soil organic matter decomposition and carbon storage in temperate
grassland. In this model, heavy grazing promotes the dominance of small-stature, fast-growing
plant species, bacterial-dominated soil communities, higher aboveground plant productivity,
faster rates of organic matter decomposition (especially of old particulate organic matter), and
lower soil carbon storage. In contrast, low grazing pressure promotes the dominance of slow-
growing, high-stature plant species, fungal-dominated soil communities, reduced rates of
organic matter decomposition, and greater soil carbon content.

negative (Bremer et al. 1998; Knapp et al. 1998; Johnson and Matchett 2001; Van der
Wal et al. 2007), positive (Ward et al. 2007), and neutral (Risch and Frank 2006;
Ward et al. 2007; Susiluoto et al. 2008) responses. However, only a handful of
studies have considered how grazing influences net ecosystem exchange (NEE),
namely the balance between net uptake of carbon dioxide by photosynthesis and
its loss by respiration, which determines whether an ecosystem is a source or sink
for carbon. One such study is that of Welker et al. (2004), who measured NEE
over two consecutive years in alpine grassland in Wyoming. They found that over
this period, rates of NEE were generally lower (i.e. lower carbon sink activity) in
grazed than ungrazed grassland, and that the grazed area was a net carbon source
of 170 g C m2, whereas the ungrazed area was a net carbon sink of 83 g C m2
(Fig. 4.20). Despite this, soil carbon stocks were greater in grazed than ungrazed
areas, indicating that integrative measures of ecosystem carbon budgets (i.e. soil
156 • 4 Significance of aboveground consumers
Ecosystem CO2 Flux (μmol CO2 m–2 sec –1)

6 6
Ungrazed
Grazed
4 4

2 2
C Sink

0 0

–2 C Source –2

–4 –4
1/1
1/18
1/22
1/29
2/10
2/23
3/14
4/1
4/22
5/12

6/12
6/23
7/2
7/15
7/21
7/29
8/12
8/28
9/6
9/12

12/12
1/6
3/3
5/7
6/3

6/20
7/8
7/28
8/20
9/12
9/18

11/12

1/6
10/
Winter 1998 Summer 1998 Winter 1999 Summer 1999 Winter 2000

Fig. 4.20 Annual net ecosystem carbon dioxide exchange (mean+1 SE) over two consecu-
tive years in ungrazed and grazed alpine grasslands in Wyoming, USA. Asterisks signify
significant differences (P < 0.05) between ungrazed and grazed treatments at a sampling date.
From Welker et al. (2004), with permission from the Institute of Arctic and Alpine Research,
University of Boulder, Colorado.

carbon contents) may not always correspond to shorter-term, instantaneous meas-

ures of carbon dioxide exchange. As noted by these authors, soil carbon seques-
tration is a dynamic process, and while the long-term trajectory might be positive
in grazed areas, periods of net carbon source activity are intermixed with periods
of when they are net sinks (Fig. 4.21). This argument is consistent with finding
that ecosystems can oscillate from being carbon sources to sinks for extended
periods in different ecosystems (Oechel et al. 1993, 1995; Flanagan et al. 2002;
Frank 2002), and that grazing can trigger short-term shifts in NEE in grassland
systems (Wohlfahrt et al. 2008).
Other studies that have compared NEE in grazed versus ungrazed areas also
point to grazer effects on NEE being driven by changes in vegetation biomass and
composition, albeit in contrasting ways. For example, Polley et al. (2008) found
that in four out of five growing seasons studied, cattle grazing of mixed prairie in
North Dakota, USA, increased mean NEE (leading to a greater carbon sink) by
reducing night-time respiration more than daytime carbon dioxide exchange.
Moreover, they found that grazing reduced inter-annual variability in mean
carbon dioxide fluxes, which was attributed to a reduction in the response of
respiration to variation in soil temperature. The mechanism for these responses
was not studied, but given that grassland respiration is greatly affected by the
availability of recently fixed carbon, and that grazing has been shown to reduce
root biomass in mixed prairie, it was suggested that grazing reduced respiration
and its responsiveness to soil temperature in part through reducing the input of
labile carbon to soil (Polley et al. 2008). Long-term grazing by sheep was also
 4.6 Aboveground consumers and global change • 157
Rate of soil carbon accumulation

Sink Grazed

Sink
Annual CO2 flux
Ungrazed
Source
Sink
Source

Source
Annual CO2 flux

Time

Fig. 4.21 Conceptual model illustrating inter-annual variation in net ecosystem carbon diox-
ide exchange as it relates to long-term carbon sequestration in grazed and ungrazed alpine
grasslands in Wyoming, USA. While both grazed and ungrazed areas have periods of carbon
gain and carbon loss, the net response is that grazed areas accumulate more soil carbon than
ungrazed areas, as indicated in the long-term trajectory. Derived from Welker et al. (2004).

found to increase NEE and hence ecosystem carbon sink strength in a study of
British peatlands by Ward et al. (2007) (Fig. 4.22). This effect, which was caused
by a greater increase in photosynthesis relative to respiration, was attributed to an
increase in the cover of fast-growing grasses relative to slower-growing dwarf-
shrubs and bryophytes, and hence a greater assimilation of carbon by the plant
community (Ward et al. 2007). In contrast, Van der Wal et al. (2007) found that
belowground foraging (i.e. grubbing) by pink-footed geese (Anser brachyr-
hynchus) reduced NEE and soil carbon stocks in high Arctic tundra in Svalbard
(Fig. 4.23). However, consistent with the above studies, this effect was attributed
to a shift in the plant community, and especially a reduction in the cover of
bryophytes and vascular plants, leading to a decline in ecosystem photosynthesis
and thus carbon gain. The decline in soil carbon stocks due to grubbing, however,
was largely attributed to the exposure of the humus layer to wind and water
erosion rather than to reduced NEE (Van der Wal et al. 2007). Finally, and in
contrast to the above studies, Susiluoto et al. (2008) found no detectable effects of
grazing by reindeer on NEE in Finnish alpine tundra, despite significant shifts in
vegetation composition. They found that lichen cover was significantly reduced
by grazing; however, lichens are relatively unproductive and contribute little to
NEE. Here, NEE was largely dependent on dwarf-shrub cover which was un-
affected by grazing, and so the overall effect of grazing on NEE was neutral.
It is important to note that year-to-year variation in ecosystem carbon budgets are
mostly attributed to climatic variability (e.g. Barford et al. 2001; Flanagan et al. 2002).
 158 • 4 Significance of aboveground consumers

NET FLUX
100
50
CO2 FLUX (mg m–2 hr–1)

0
–50
–100
–150
–200
–250
–300
03

Ju 03

ug 3
03

O 03

03

03

Ja 03

Fe 04

04

04

04

Ju 04

04

04
0
20

20

20

20

20

20

20

20

20

20

20

20

20

20

20
ay

ne

ly

pt

ct

ov

ec

ar

pr

ay

ly

pt
D
Se

Se
A
Ju
M

M
A

SAMPLE DATE

Fig. 4.22 Influence of grazing on net ecosystem carbon dioxide exchange over two growing
seasons in peatland the north of England. Values are means+SE. Positive values indicate a net
loss of carbon dioxide and negative numbers imply carbon uptake. Filled bars are grazed plots
whereas empty bars are ungrazed plots. Data from Ward et al. (2007), with permission from
Springer ScienceþBusiness Media.

However, it is becoming apparent that grazing (and presumably other biotic factors) not
only affects ecosystem carbon exchange, but also alters the influence of climate on
land–atmosphere carbon fluxes. For instance, in the abovementioned study of Polley
et al. (2008), grazing was found to change the identity of the primary climatic driver of
year-to-year variability in carbon dioxide flux, and to alter the responsiveness of
respiration to soil temperature. Likewise, while climatic factors were the main factor
explaining seasonal variation in gross and net fluxes of carbon dioxide in the above-
mentioned study of Ward et al. (2007), significant grazer effects were detected and,
moreover, they altered the seasonal dynamics of net and gross carbon fluxes. As argued
by Polley et al. (2008), these findings indicate that predictive models need to accom-
modate biotic factors such as grazing in order to accurately simulate the dynamics of
carbon dioxide fluxes in terrestrial ecosystems. However, this is hampered by a lack of
understanding of the relative roles of climatic versus biotic drivers of carbon dynamics,
and the potential for grazing (and other biotic factors) to modulate the response of
carbon flux to climatic variability and hence climate change.
Very few studies have experimentally tested the relative role of herbivory and
climate change in driving carbon fluxes in terrestrial ecosystems. One such study, by
Sjögersten et al. (2008), examined the combined roles of herbivory (by captive
Barnacle geese, Branta leucopsis) and climate warming (through open-top chambers)
as drivers of carbon dioxide fluxes in two Arctic habitats, namely mesic heath and wet
tundra. They found that in wet tundra, goose grazing significantly reduced NEE of
carbon dioxide (and hence carbon sink strength) while warming had little impact
during the growing season. However, warming did increase carbon dioxide efflux
 4.6 Aboveground consumers and global change • 159

(a) Net ecosystem exchange (NEE)

–0.5

b
–1.0
b
–1.5

–2.0
a

(b) Gross ecosystem photosynthesis (GEP)

Carbon flux (mmol Cm–2 s–1)

–1.0

–2.0 b
b
–3.0

–4.0 a

(c) Ecosystem respiration (Re)

2.0 a
ab
1.0 b

C G E

Fig. 4.23 Impact of goose grubbing on (a) carbon dioxide NEE, (b) gross ecosystem photo-
synthesis (GEP), and (c) ecosystem respiration (Re) in Arctic tundra. Data are means+SE for
an intact control (C), goose-grubbed (G), and experimentally grubbed (E) wet tundra. Negative
numbers imply carbon uptake and positive numbers imply carbon losses from the system.
Values with different letters are significantly different at the P < 0.05 level. Data from Van der
Val et al. (2006), with permission from Wiley-Blackwell.

from wet tundra during the winter, further contributing to carbon loss from the
system. In the mesic heath, warming reduced carbon dioxide efflux, and the com-
bination of warming and low-level grazing altered the carbon balance during the
growing season from a source to a weak net sink of carbon dioxide. Collectively,
these results indicate that grazing by geese can result in either increased or decreased
carbon sink strength in the high Arctic, depending on the habitat and climatic
160 • 4 Significance of aboveground consumers

conditions; however, in agreement with Van der Wal et al. (2007), grazing exerted the
strongest negative effect on carbon dioxide sink strength in wet tundra. The negative
effect of grazing on NEE at the wet site (which is the type of feeding ground preferred
by geese), was attributed to declines in aboveground plant biomass, and hence carbon
assimilation by photosynthesis. In contrast, the interactive effect of warming and
grazing at the mesic site was likely due to increased plant biomass and hence
assimilation of carbon dioxide caused by both warming and grazing (Sjögersten
et al. 2008). Overall, this study indicates that grazing has the potential to modulate
the effects of climate warming on the ecosystem carbon balance, but that this effect is
site specific and strongly driven by vegetation responses.
Two other studies on the combined effects of grazing and warming also indicate
the potential for grazers to modulate the effects of climate change on plant commu-
nities and belowground processes, albeit not in the context of carbon dioxide fluxes.
First, Rinnan et al. (2009) performed a factorial warming and herbivory-simulation
(clipping) experiment in Finnish sub-Arctic tundra, and showed that long-term
warming enhanced the growth of the dominant dwarf-shrub Vaccinium myrtillus
and reduced soil ammonium-nitrogen availability and microbial immobilization of
nitrogen only in the absence of simulated herbivory. These results point to the role of
defoliation in modulating the responses of both plants and soil microbes to warming.
Second, Post and Pedersen (2008) incorporated natural herbivory by muskoxen and
caribou into a 5-year experimental investigation of Arctic plant community response
to warming in West Greenland. In accordance with other studies, they found that
warming increased total community biomass by promoting growth of birch (Betula
nana) and willow (Salix glauca). However, muskoxen and caribou grazing reduced
the total community biomass response to warming by 19%, and the response of birch
and willow by 46 and 11% respectively. Further, under warming alone, the plant
community shifted after 5 years from graminoid-dominated towards dwarf birch-
dominated. In contrast, when herbivory was present, plant community composition
on warmed plots after 5 years did not differ from that on ambient plots. These results,
along with those of Rinnan et al. (2009) and Sjögersten et al. (2008), highlight the
potentially important and often overlooked influences of herbivores on plant com-
munity and belowground responses to warming. As noted by Post and Pedersen
(2009), conservation and management of herbivores may therefore be an important,
though little understood, component of mitigating ecosystem responses to climate
change.
As highlighted recently by Wookey et al. (2009), climate change-induced shifts in
the functional composition of vegetation also have the potential to affect herbivore
populations through a variety of mechanisms. First, large-scale shifts in vegetation
productivity, phenology and composition will substantially alter the quantity, qual-
ity, and temporal availability of herbivore diet, thereby affecting herbivore perform-
ance and behaviour. Second, climate-induced alteration of growth and allocation
patterns in individual plant functional types, for example in terms of secondary
metabolite production and allocation to foliage, will alter the quality and quantity of
forage (Coley et al. 1985). Third, the potential direct effects of climate change,
 4.7 Conclusions • 161

together with changes mediated by shifts in vegetation composition, will influence

soil biological properties that regulate the availability of nutrients to plants, thereby
creating a potential feedback on plant productivity and forage supply (Bardgett and
Wardle 2003). Finally, changes in vegetation composition will modify habitat
availability and architecture, and spatial arrangement, with potential effects for
herbivores and fauna that use plants for habitat, such as rodents, insects, and birds
(Wookey et al. 2009).
Such indirect effects of climate change on herbivore performance and behaviour
could in turn feedback to the plant community and the belowground subsystem, and
serve to inhibit or facilitate vegetation change. For example, evidence from long-term
studies in northern-temperate elk/aspen (Cervis canadensis/Populus tremuloides) and
moose/balsam fir (A. alces/Abies abies) systems suggests that woody-plant expansion
in response to warming might be constrained by large herbivores (Post et al. 1999;
Ripple and Betscha 2004), and recent studies in the Arctic likewise suggest that shrub
expansion due to warming might be limited by reindeer grazing (Olofsson et al.
2009). Moreover, climate-induced changes in vegetation productivity and compos-
ition could exert multitrophic effects aboveground, influencing densities of not just
herbivores, but also their predators. Changes in predator numbers or behaviour in
response to climate change are in turn likely to cause cascading effects on ecosystem
properties by further modulating herbivore effects on vegetation change and resulting
feedback mechanisms (Terborgh et al. 2001; Creel et al. 2005; Gunn et al. 2006). As
discussed earlier in this chapter, these cascading effects have the potential to indir-
ectly influence belowground food webs and the ecosystem processes that they drive.
However, the impact of climate change on multitrophic feedbacks between the
aboveground and belowground subsystems, and the consequences of this for ecosys-
tem functioning, remains essentially unexplored.
Clearly there is much to be learned about the response of herbivores and other
trophic groups to climate change and the consequences of this for ecosystem pro-
cesses, including ecosystem carbon exchange and carbon-cycle feedbacks. Such
responses are likely to be complicated and site-specific, but as illustrated in this
and the preceding section, they are likely to play a significant role in modulating the
response of ecosystems to climate and other global changes. Given the dearth of
studies in this area, there is a clear need for more research aimed at an improved
understanding of how herbivores, and other biotic factors, modulate ecosystem
responses to climate change, and ultimately how herbivore management might be
altered to mitigate climate change.

4.7 Conclusions
In this chapter we have examined how aboveground consumers, including mam-
malian and invertebrate herbivores and their predators, affect the belowground
subsystem through a variety of mechanisms, with often far-reaching consequences
for the structure and functioning of terrestrial ecosystems. Moreover, we have
162 • 4 Significance of aboveground consumers

examined these responses in a global change context, exploring how herbivores can
modulate terrestrial ecosystem carbon cycling with potential consequences for
carbon-cycle feedbacks and climate change. Although it has been recognized for
some time that aboveground herbivores can strongly modulate ecosystem processes
through their influence on the belowground subsystem, there have been several
important recent advances in understanding in this area. Not only has our know-
ledge of the various mechanisms by which herbivores influence the belowground
subsystem and aboveground–belowground feedbacks improved, but there is also a
growing understanding of the relative importance of these different mechanisms,
both biotic and abiotic, in explaining belowground and ecosystem-level responses
to herbivory (Mikola et al. 2009; Sørensen et al. 2009; Veen et al. 2010). Our
understanding of the influence of aboveground consumers on ecosystem properties
has also extended to consider the multitrophic linkages. In particular, there is
growing recognition that aboveground predators of herbivores can induce trophic
cascades that affect the functioning of the belowground subsystem with conse-
quences for ecosystem functioning (e.g. Feeley and Terborgh 2005; Wardle et al.
2005; Maron et al. 2006; Schmitz 2008a; Wardle 2010).
Another advance has been an improved mechanistic and predictive understanding
about why different ecosystems differ in their response to herbivory. This has been
helped through an improved understanding of plant trait responses to grazing (e.g.
Díaz et al. 2006), which we argue could provide a framework for investigating
feedbacks between grazers, plants, soil organisms, and nutrient cycles, and how
they vary across environmental gradients such as soil fertility and climate. Further
evidence that we present in this chapter supports the notion that a conceptual
framework for investigating plant trait responses to herbivory could be extended to
incorporate belowground responses, and hence provide a basis for improved under-
standing the consequences of herbivory for ecosystem function in different contexts.
Another important and related development has been an improved understanding of
how herbivore impacts vary across environmental gradients at the landscape scale,
for instance of soil fertility, topographic position, and climate (Augustine and
McNaughton 2006; Anser et al. 2009). Moreover, there is growing recognition that
herbivores can force predictable shifts in vegetation state at the landscape scale, with
both catastrophic negative (Rietkerk and van de Koppel 1997) and positive (Van der
Wal 2006) consequences for their functioning and carrying capacity. Studies in these
topics are still in their infancy, and further work is needed to better understand
how herbivore effects on ecosystem processes that are becoming increasingly well
understood at local spatial scales may be manifested at the landscape scale.
A related development is the recognition that herbivore movements during for-
aging and associated transfers of resources across sites as animal wastes can have
significant consequences for landscape-scale spatial patterns of nutrient cycling and
vegetation. Most work on this issue has historically been done in agricultural
situations, where livestock can promote patchy return of nutrients through using
different parts of their habitat for feeding and for excretion. As a result, nutrients
become concentrated in relatively small areas where animals spend a large amount of
 4.7 Conclusions • 163

their time (Afzal and Adams 1992; Kohler et al. 2006; Jewell et al. 2007). However,
there is growing evidence that wild herbivores can also influence nutrient transloca-
tion and the spatial distribution of soil nutrients in natural ecosystems, with long-term
consequences for the spatial dynamics of vegetation (e.g. Augustine and Frank 2001;
Yang 2004; Schütz et al. 2006). Moreover, there is emerging evidence that carcasses
of vertebrate and invertebrate herbivores have significant and lasting effects on the
functioning terrestrial ecosystems, by creating pulses of nutrients into the soil which
create spatial heterogeneity in nutrient cycling and vegetation at the landscape scale
(Towne 2000; Yang 2004; Bump et al. 2009a, 2009c; Parmenter and MacMahon
2009). Also, as shown by Bump et al. (2009a), such spatial heterogeneity in terrestrial
ecosystems can be modulated by predators, whose behaviour influences the spatial
distribution of carcasses and their impact on ecosystem processes; such findings
further emphasize the important roles that predators play in modulating the function-
ing of terrestrial ecosystems. There is also growing recognition that aboveground and
belowground components of terrestrial ecosystems are affected by both aquatic and
terrestrial consumers that transfer resources from water to land. For example, the
input of seabird guano to terrestrial ecosystems can have strong positive effects on
soil nutrient availability (Polis and Hurd 1996; Mulder and Keall 2001; Fukami et al.
2006) and the abundance of soil organisms (Towns et al. 2009), resulting in enhanced
plant nutrient acquisition and growth (Anderson and Polis 1999; Fukami et al. 2006;
Maron et al. 2006; Mulder et al. 2009), and increased plant litter quality (Wardle et al.
2009b). Similarly, the capture of salmon from rivers by bears, and their subsequent
transport into adjacent riparian forests, can serve as a significant nitrogen input in
these forests, with consequences for local patterns of soil nitrogen availability, plant
nutrient uptake, and ultimately browsing patterns of herbivores (e.g. Helfield and
Naiman 2006; Gende et al. 2007). As we stress in this chapter, however, studies of the
impact of aquatic organisms on the structure and function of adjacent terrestrial
ecosystems are still at their infancy, so generalizations about the extent to which
aquatic to terrestrial inputs are important are still poorly understood.
As highlighted in both this and the preceding two chapters, a topic that has
attracted much recent attention is the role that biotic interactions play in regulating
carbon dynamics in terrestrial ecosystems, especially in the context of land–atmosphere
carbon exchanges and carbon-cycle feedbacks that could impact on climate change. It
is clear from this chapter, for example, that climate change-induced shift in vegetation
composition can affect herbivore populations, which could in turn feedback to the
plant community and the belowground subsystem, thereby inhibiting or facilitating
vegetation change (Wookey et al. 2009). Moreover, recent studies indicate that
herbivores themselves can modulate the effects of climate change on plant commu-
nities and belowground processes (Rinnan et al. 2009; Olofsson et al. 2009; Post and
Pedersen 2009), suggesting that conservation and management of herbivores may be
an important, though little understood, component of mitigating ecosystem responses
to climate change (Post and Pedersen 2009). Another important development in this
general area is the recognition that grazing (and presumably other biotic factors) not
only affects ecosystem carbon exchange, but also alters the influence of climate on
164 • 4 Significance of aboveground consumers

land-atmosphere carbon fluxes (Polley et al. 2008). Although more studies are needed
in this area, this finding is especially important because it indicates that predictive
models need to accommodate biotic factors such as grazing in order to accurately
simulate the dynamics of carbon dioxide fluxes in terrestrial ecosystems. However,
this is hampered by a lack of understanding of the relative roles of climatic versus
biotic drivers of carbon dynamics, and the potential for grazing (and other biotic
factors) to modulate the response of carbon flux to climatic variability and hence
climate change. Given this, there is a clear need for more research aimed at an
improved understanding of how herbivores, and other biotic factors, modulate
ecosystem responses to climate change, and ultimately how herbivore management
might be altered to mitigate climate change.
5
Aboveground and belowground
consequences of species losses and gains

5.1 Introduction
In Chapters 2–4 we discussed three major groups of biotic drivers of terrestrial
ecosystem functioning, namely the belowground biota, the plant community, and
the aboveground consumers. We also explored the ecological significance of changes
in community composition within each of these groups of biotic drivers resulting
from human-induced atmospheric global change phenomena, such as climate change
and nitrogen deposition. However, global change also involves biotic interchange,
resulting from both the loss and gain of species in the community (Vitousek et al.
1997b). This occurs on two fronts. First, human activity is contributing to significant
extinctions of species on both local and global scales, and it is widely recognized that
the Earth is undergoing its sixth major extinction event. Indeed, for many groups of
biota, the current rate of extinction of species is probably around 100–1000 times
their pre-human levels (Pimm et al. 1995; Millennium Ecosystem Assessment 2005).
These species losses are a consequence of several human-induced factors, the most
important of which is arguably habitat destruction and land-use change (Sala et al.
2000). However, other important causes of species loss include climate change
(Thomas et al. 2004; Thuiller et al. 2005), nitrogen deposition (Stevens et al. 2004;
Phoenix et al. 2006), invasive predators (Beggs and Rees 1999; McKinney and
Lockwood 1999), and harvesting of desirable plant and animal species (Bodmer
et al. 1997; Wardle et al. 2008c). Second, human migration throughout the world has
greatly facilitated the introduction of plant and animal species to new habitats; these
introductions have been both accidental and deliberate, and have frequently led to
biological invasions of natural ecosystems. Ecological changes caused by biological
invasions have occurred whenever humans have colonized new land, and are cur-
rently occurring most rapidly on the most recently settled land masses, such as New
Zealand (Allen and Lee 2006) and Hawai’i (Vitousek et al. 1997b). Further, many
ecosystems are losing some species through extinction and gaining others through
invasion, and therefore the net result can be either a net gain or net reduction in
species depending on context (Sax and Gaines 2003; Sax et al. 2005; Phoenix et al.
2006; Van Calster et al. 2008).
When species are gained by or lost from a community, there can be important
consequences for both the aboveground and belowground subsystems, especially
166 • 5 Consequences of species losses and gains

when these species differ in key functional attributes from the rest of the community.
Some of the more extreme effects of species loss or gain are widely known.
For example, extinction of megaherbivore populations can lead to major shifts in
vegetation type and soil fertility (Zimov et al. 1995; Wardle and Bardgett 2004).
Similarly, invasions of ecosystems by novel types of organisms such as top predators
(O’Dowd et al. 2003; Fukami et al. 2006) or nitrogen-fixing plants (Vitousek and
Walker 1989) can induce fundamental shifts in both aboveground and belowground
ecosystem processes. However, although these represent extreme cases driven by
losses or gains of species with key attributes, more subtle ecological effects of species
extinctions and invasions might be widespread. In this light, there is growing
evidence for communities of both animals (e.g. Bodmer et al. 1997; Cardillo et al.
2005) and plants (e.g. Duncan and Young 2000; Van Calster et al. 2008) that those
species lost through extinction may collectively differ in particular traits or attributes
from those that are not lost. Similarly, for plant communities at least, comparative
studies often point to significant differences in key traits between the native and alien
components of the resident flora (e.g. Funk and Vitousek 2007; Leishman et al. 2007).
When the traits that differ between invasive and non-invasive species, or between
species that vary in their susceptibility to extinction, are the same as those traits which
influence key ecological processes, there is the potential for changes in ecosystem
functioning to occur.
The goal of this chapter is to outline the changes in aboveground and belowground
communities, and the ecosystem processes that they drive, that occur as a conse-
quence of biotic interchange. To do this, we first discuss how species losses from
communities may affect aboveground and belowground biota and ecosystem prop-
erties, and hence how biological extinctions may impact upon ecosystems. We will
then outline the consequences of ingress of new species into communities for the
aboveground and belowground components of ecosystems. Finally, we discuss how
global change phenomena affect aboveground and belowground properties and
organisms through causing gains or losses of key species. In doing this, our overall
goal is to draw upon the concepts developed in Chapters 2–4 to better understand
how biotic interchange affects ecosystems by influencing aboveground–belowground
linkages.

5.2 Species losses through extinction

and aboveground–belowground linkages
5.2.1 The diversity-function issue from an aboveground–
belowground perspective
The issue of how variation in species richness of organisms may affect the rates and
stability of ecosystem processes (e.g. productivity, decomposition and nutrient cyc-
ling) has long been a research focus of both agronomists (e.g. Trenbath 1974;
Vandermeer 1990) and ecologists (e.g. Odum 1969; McNaughton 1977). However,
 5.2 Species losses through extinction • 167

since the mid-1990s, components of this topic have attracted substantial attention
from ecologists and have also generated a considerable amount of debate (Huston
1997; Kaiser 2000; Hooper et al. 2005). Over that time, many experimental studies
have been performed to study this topic, mostly involving the setting-up of artificial
communities in which organism diversity (usually at the species or functional-group
level) is experimentally varied (often by drawing random assemblages of species
from a pool of species), with ecosystem response variables then being monitored over
time. Various points of view have been expressed as to how relevant such studies are
for understanding the effects of human-driven species losses in real ecosystems
(Huston 1997; Tilman 1999; Wardle 1999; Leps 2004; Ridder 2008; Duffy 2009).
Because studies investigating biodiversity effects on ecosystem functioning fre-
quently interpret their results in terms of the ecological consequences of species
extinctions, we provide a brief overview of the current state of knowledge of this
topic, especially in the context of aboveground–belowground linkages. We empha-
size that it is not possible to provide an exhaustive review of the topic given the
volume of recent literature on it; as such, our choices of examples are representative,
not exhaustive. For more detailed treatment we refer the reader to reviews by Hooper
et al. (2005), and for the belowground subsystem Wardle and Van der Putten (2002)
and Hättenschwiler et al. (2005).
The effects of plant species or functional-group richness (or other measures of
diversity) on NPP have been extensively investigated. Many experimental studies
have found positive effects of diversity on NPP (see Balvanera et al. 2006; Cardinale
et al. 2006), although the interpretation and mechanistic basis underlying the results
of these studies continues to be debated (Hooper et al. 2005). Further, the importance
of richness as a driver of productivity varies greatly among and even within studies
(Fridley 2002; Hooper and Dukes 2004), and may be only minor in natural ecosys-
tems when compared to other biotic and abiotic factors (e.g. Wardle et al. 1997b;
Grace et al. 2007). For those studies that do point to positive effects of live plant
diversity on NPP (see Balvanera et al. 2006; Cardinale et al. 2006), an increased
quantity and diversity of resources should in turn enter the belowground subsystem,
potentially stimulating decomposer organisms and processes through various mech-
anisms (Fig. 5.1). However, of the 30 or more studies to date that have explicitly
investigated the effects of plant diversity on the performance of the decomposer
subsystem, the vast majority have found diversity to have weak or non-existent
effects, and most of these have instead shown plant species identity to be the main
belowground driver (e.g. Wardle and Van der Putten 2002; Porazinska et al. 2003;
Hedlund et al. 2003; De Deyn et al. 2004). A small number of experimental studies
have detected a strong effect of plant diversity on the decomposer subsystem (notably
Stephan et al. 2000 and Zak et al. 2003), but in those cases plant diversity also had
strong effects on NPP and therefore presumably the input of resources belowground.
The fact that most studies involving experimental manipulation of plant diversity find
some positive effects on NPP, but little or no consistent effect on belowground
organisms and their activities, is reflective of relatively weak or inconsistent coupling
between the producer and decomposer subsystems.
168 • 5 Consequences of species losses and gains

Increased plant
diversity

Plant resource use Root exudate

Positive Plant litter
complementarity biochemical
interactions (+) diversity (+)
(+) diversity (+)

Decomposer
NPP (+)
diversity (+)

Detrital and root Decomposer

Plant nutrient
exudate resource use
uptake (+)
quantity (+) complementarity (+)

Microbial biomass Microbial biomass

and soil fauna and soil fauna
(–) (0, +)

Short-term decomposition Long-term accumulation

and nutrient mineralisation of detritus
(–, 0, +) (–, 0, +)

Nutrient supply
to plants
(–, 0, +)

Fig. 5.1 Hypothesized mechanisms by which increasing plant species diversity may affect
decomposer-mediated processes. Symbols: þ, 0, and  indicate positive, neutral, and negative
effects, respectively. From Wardle and van der Putten (2002), with permission from Oxford
University Press.

As discussed in Chapter 3, plants affect the belowground subsystem not only when
they are alive, but also through ‘afterlife effects’ manifested through the litter that
they produce. Therefore, the question emerges as to what effects plant litter diversity
might exert on the decomposer subsystem. This has been extensively studied through
the so-called litter mixture experiments in which the decomposition of plant litter in
multiple species mixtures is compared with that of the component species decom-
posed singly. Such an approach has now been used in well over 50 studies (see
Wardle and Van der Putten 2002; Gartner and Cardon 2004), and collectively these
studies show highly variable effects of litter mixing on litter-mass loss, ranging from
 5.2 Species losses through extinction • 169

strongly positive to strongly negative, although positive (i.e. synergistic) effects of

litter mixing are more numerous than negative effects (Gartner and Cardon 2004).
The mechanistic basis of litter-mixing effects remains elusive, and evidence is mixed
as to whether or not non-additive mixing effects become greater when litter types are
more dissimilar in terms of their quality (Wardle et al. 1997a; Hoorens et al. 2003;
Quested et al. 2005). Further, litter mixing can influence the density of decomposer
organisms, though not in an easily predictable way (Hansen 2000; Wardle 2006). For
example, Blair et al. (1990) found that litter mixing often promoted the density of
fungivorous nematodes, but reduced the density of mesofaunal groups, living within
the litter (Fig. 5.2). Finally it is important to note that decomposer invertebrates can in
turn greatly influence the magnitude of non-additive litter-mixing effects on mass loss
(Hättenschwiler and Gasser 2005; Schädler et al. 2005), pointing to the possibility of
complex interactions between multiple plant species and the decomposer community
in regulating decomposer processes.
As highlighted in Chapter 2, soil organisms also have a major role in driving
belowground processes that influence nutrient availability and therefore plant growth.
The issue therefore emerges as to whether diversity of detritivorous organisms affects
processes in the soil that may impact on aboveground organisms and processes. There
is a modest but growing number of studies that have explicitly addressed the effects
of decomposer diversity on soil processes (Wardle 2002; Hättenschwiler et al. 2005).
For example, and as also emphasized in Chapter 2, there is some evidence that
decomposition of organic materials and other related soil processes can be positively
influenced by the species diversity of saprophytic fungi (Robinson et al. 1993; Setälä
and McLean 2004; Tiunov and Scheu 2005) and arthropods (Liiri et al. 2001),
probably through different taxa preferentially utilizing different organic substrates
and leading to greater resource use complementarity. However, these effects are
mostly apparent at the low-diversity end of the spectrum (see Chapter 2), and at
levels of diversity that are likely to be well below that which is found in real
ecosystems (Wardle 2002). There has to date been little exploration of how decom-
poser diversity effects on soil processes might in turn indirectly influence above-
ground processes, such as plant nutrient acquisition and growth. However, as
discussed in Chapter 2, Laakso and Setälä (1999a) found little effect of soil meso-
faunal species diversity on growth of Betula pendula seedlings, and Cole et al. (2004)
showed that nitrogen acquisition by the grass Agrostis capillaris was unresponsive to
soil microarthropod species richness.
A handful of studies have also focused on the aboveground effects of the diversity
of soil organisms that interact with plants through the direct pathway. As discussed in
Chapter 2, some studies have investigated the effects of diversity of ectomycorrhizal
fungi (Jonsson et al. 2001) or arbuscular mycorrhizal fungi (Van der Heijden et al.
1998b; Vogelsang et al. 2006; Maherali and Klironomos 2007) on plant growth, and
have collectively documented responses ranging from strongly positive to neutral,
even within the same study (Jonsson et al. 2001). Despite the likely importance of root
pathogens and root herbivores as regulators of plant growth (Chapters 2 and 3), little is
known about how the diversity of these organisms impact upon plants. However, in a
170 • 5 Consequences of species losses and gains

Expected Observed: Cornus/Acer

P/O P/O
P P

BF FF M BF FF M

O O
B F B F

C C
Litter Litter

Observed: Acer/Quercus Observed: Cornus/Acer/Quercus

P/O P/O
P P

BF FF M BF FF M

O O
B F B F

C C
Litter Litter

Fig. 5.2 Effects of plant litter diversity on microbial and faunal components of the detritus food
web inhabiting the litter, in a forest ecosystem in Georgia, USA. For each component, the area of
each square or rectangle represents its observed mass or population in two- or three-species litter
mixes, relative to expected values derived from litter monocultures, assuming effects of all litter
types are purely additive. B, bacteria; F, fungi; BF, bacterial-feeding nematodes; FF, fungal-feeding
nematodes; P/O, predatory/omnivorous nematodes; C, Collembola; O, oribatid mites; M, mesos-
tigmatid mites; P, protostigmatid mites. Calculated from data of Blair et al. (1990), as presented by
Wardle and Lavelle (1997), with permission from CAB International.

study in which species richness of root-feeding nematodes was experimentally varied,

Brinkman et al. (2005) found that growth of the dune plant Ammophila arenaria was
influenced primarily by the identity of the nematodes, rather than the number of
species present. This is consistent with other studies showing plant growth to be
responsive to species identity of root-feeding nematodes (Wurst and Van der Putten
2007) and root pathogenic fungi (De Rooij-van der Goes 1995). Little is also known
about the ecological effects of diversity of soil bacteria that perform specialized
belowground functions, such as nitrogen fixation and nitrification. However, these
types of function are often performed by a physiologically and/or phylogentically
 5.2 Species losses through extinction • 171

narrow range of taxa, when compared to ‘broad’ processes such as nitrogen mineral-
ization (Schimel et al. 2005). Hence, it is generally thought that processes such as
nitrogen fixation and nitrification will be more sensitive to changes in microbial
community composition and diversity than is nitrogen mineralization. For example,
symbiotic nitrogen fixation in legumes is characteristically performed by a small
number of strains of Rhizobium, and losses of a subset of these strains can greatly
impair symbiotic nitrogen fixation and legume growth (Giller et al. 1998).
Despite the importance of aboveground consumers (foliar herbivores and their
predators) in driving the aboveground and belowground subsystem (see Chapter 4),
we are not aware of any studies that have investigated how the diversity of soil
organisms may affect the performance of aboveground consumers. Further, despite
growing interest in how consumer diversity may drive ecosystem functioning (Johnson
2000; Duffy et al. 2007), the belowground consequences of aboveground consumer
diversity has received scant attention. It is, however, theoretically possible for
herbivore diversity to either increase or decrease the densities of belowground
organisms and rates of soil processes, depending on the mechanisms involved
(Bardgett and Wardle 2003). In the one study to date that has investigated this
issue, Wardle et al. (2004c) performed a microcosm experiment in which the diver-
sity of foliar-feeding aphids was experimentally varied from one to eight species.
Although aphid species identity emerged as an important driver of both the plant
community and multiple trophic levels of the soil food web, aphid species richness
had few effects, and those that did occur were at the low-diversity end of the spectrum
(two versus one species).
There is a long-standing interest in how biodiversity affects not just ecosystem
processes, but also their stability. As such, even when species richness may be
unimportant as a driver of ecosystem processes at a given point of time, the possi-
bility remains that richness may influence the temporal dynamics of the ecosystem
through altering its resistance and resilience to external perturbation (Hooper et al.
2005). There is a long history of theoretical studies (May 1973; McNaughton 1977)
and many empirical studies (e.g. Sankaran and McNaughton 1999; Tilman et al.
2006; Bezemer and Van der Putten 2007) that have explicitly addressed this issue.
A detailed discussion of this topic is beyond the scope of this book, and we refer the
reader to reviews of this topic by Cottingham et al. (2001), Hooper et al. (2005) and
Ives and Carpenter (2007). It is notable that the effect of organism species richness on
the temporal variability of belowground organisms and processes has seldom been
explored. However, controlled glasshouse studies by Wardle et al. (2000) and Orwin
and Wardle (2005) provide evidence that while plant species richness has some
positive effects on NPP, the stability of a range of aboveground and belowground
properties, assessed by measuring ecosystem responses to an experimentally applied
drying disturbance, was unaffected by plant diversity. Moreover, both these studies
found that the stability of these properties was influenced by plant species identity,
which is consistent with other studies that have shown plant species identity and
functional attributes influence the temporal variability of aboveground and below-
ground properties (MacGillivray et al. 1995; Wardle et al. 1999).
172 • 5 Consequences of species losses and gains

In sum, when the diversity-function issue is considered from a combined above-

ground–belowground perspective, there is considerable variability among studies:
some studies find strong effects of diversity on ecosystem properties, whereas others
find weak, neutral, or inconsistent effects. This conclusion contrasts to that drawn
from recent meta-analyses of experimental studies on diversity-function relationships
(e.g. Balvanera et al. 2006; Cardinale et al. 2006), and it has been claimed that those
analyses show diversity effects to be ‘surprisingly consistent across taxa, trophic
levels and habitats’ (Duffy 2009). However, given the wide variability among studies
in terms of experimental design, levels of diversity used, and results obtained, it is
unlikely that meta-analyses of this kind would have the statistical power to identify
important differences that exist in diversity-function relationships between taxa or
habitats (Wardle and Jonsson 2010). Further, diversity-function relationships are
themselves driven by the balance of resource partitioning, competition, and facilita-
tion among coexisting species, and this balance in turn varies greatly across both
habitat and taxa. As such, there are good theoretical reasons for predicting that the
relationship between diversity and function should not be consistent (Wardle and
Jonsson 2010). The most powerful means of looking at the effect of habitat condi-
tions on the diversity-function relationship is to experimentally vary both habitat
factors and diversity within the same study. A handful of studies that are relevant to
understanding aboveground–belowground linkages have taken precisely this ap-
proach, and these consistently show that the effect of diversity on ecosystem pro-
cesses depends strongly on environmental context (Fig. 5.3). These include studies
that have shown that the effects of litter diversity on the rate of decomposition are
influenced by other trophic levels (Hättenschwiler and Gasser 2005; Schädler et al.
2005) and soil fertility (Jonsson and Wardle 2008), that the effects of live plant
diversity on NPP depends on soil fertility (Fridley 2002) and other trophic levels
(Mulder et al. 1999), and that the effects of mycorrhizal fungal diversity on host plant
growth depends on both soil fertility and host plant species (Jonsson et al. 2001).

5.2.2 Removal experiments for studying effects of species losses

As discussed above, a large number of studies have reported experiments involving
random assemblages of species that vary in species richness, and many of them have
claimed to be directly relevant to understanding the consequences of human-induced
extinctions in real ecosystems. However, in reality, communities do not consist of
random assemblages of species, and species are not lost at random from communities
during local extinction (Wardle 1999; Solan et al. 2004; Zavaleta and Hulvey 2004).
As a consequence, the relevance of studies that involve random assemblages of
species for understanding the effects of human-driven species losses in real ecosys-
tems and for conservation management has been questioned (Huston 1997; Leps
2004; Ridder 2008). During both local and global extinction events, species with
particular traits are often lost from a community more readily than others (Cardillo
et al. 2005; Van Calster et al. 2008). Importantly, losses of species from a community
are more likely to influence the functioning of that community when those traits that
 5.2 Species losses through extinction • 173

(a) Plant diversity (b) Plant diversity (c) Litter diversity effects
effects on NPP effects on soil on decomposition
processes
(ii)

(i)
Magnitude of effect of biodiversity on
ecosystem processes

Nutrient availability Nutrient availability Nutrient availability

(d) Litter diversity effects (e) Plant diversity (f) Mycorrhizal fungal
on decomposition effects on NPP diversity effects on plant
growth
(i)

(ii)

Density of Density of invertebrate Nutrient availability

macroinvertebrates herbivores

Fig. 5.3 Studies showing that the magnitude or occurrence of effects of biodiversity on
ecosystem level processes (vertical axes) depends upon environmental context such as soil
fertility and organisms in other trophic levels (horizontal axes). Curves depict only the
directions of trends and do not reflect relative magnitude or precise shape of the curve. Data
are sourced from: (a) Fridley (2002); (b) Wardle and Zackrisson (2005); (c) Jonsson and
Wardle (2008), where (i) ¼ plots without shrubs and (ii) ¼ plots with shrubs; (d) Schädler and
Brandl (2005); (e) Mulder et al. (1999); and (f) Jonsson et al. (2001), where (i) ¼ Pinus as host
plant and (ii) ¼ Betula as host plant.

predispose particular species to extinction are also those that are important in driving
ecosystem processes. For example, atmospheric nitrogen deposition results in the
disproportionate loss of species with functional attributes that also influence nutrient
cycling and promote conservation of nutrients within the ecosystem (Berendse 1998;
Nilsson et al. 2002). Similarly, those species that are most likely to be lost through
exploitation, for example through tree harvesting (Wardle et al. 2008c) or over-
hunting (Zimov et al. 1995), are likely to disproportionately influence ecosystem
processes because they are often the biomass dominants within their trophic level.
The ecosystem-level effects of these sorts of non-random losses are not captured in
experiments in which communities are assembled at random. However, a growing
number of studies are employing alternative approaches, such as the non-random
experimental removals of species or functional groups, to better understand what
happens when species are lost from natural ecosystems in a non-random manner
(reviewed in Díaz et al. 2003). Such removal experiments have employed various
approaches to remove most main groups of terrestrial biota from communities,
including plants, microbes, soil fauna, and aboveground animals (Fig. 5.4).
174 • 5 Consequences of species losses and gains

Aboveground Fenced exclusion

vertebrates plots

Physical removal or
Plants
weeding, biocides

Increasing
temporal
Invertebrate Exclusion cages,
and spatial
herbivores biocides
scale

Exclusion by mesh,
Soil biocides, freezing,
invertebrates electroshocking
(earthworms)

Soil Selective disturbance,

microbes dilution, biocides

REMOVAL
ORGANISM
APPROACH

Fig. 5.4 Approaches that have been used for studying the ecosystem effects of removals of
organisms at contrasting spatial and temporal scales.

Removal experimental approaches applied to the plant community usually involve

physical removal of key species or functional groups. Removal approaches have long
been used for studying plant–plant interactions such as competition and facilitation
(e.g. Abdul-Fatih and Bazzaz 1979; Armesto and Pickett 1985), but are increasingly
being used for determining the consequences for ecosystem processes of losses of
subsets of the resident flora (Díaz et al. 2003) (Fig. 5.5). For example, Wardle et al.
(1999) performed a removal experiment in a grazed grassland ecosystem in New
Zealand to show that losses of the main plant functional groups in the community (all
C3 grasses, annual C3 grasses, C4 grasses, forbs) sometimes exerted important effects
on the composition of the soil biotic community, with C3 grasses usually having the
 5.2 Species losses through extinction • 175

(a) (b)

(c) (d)

Fig. 5.5 Removal experiments for studying the effects of plant species losses on ecosystem
properties. (a, b) Ongoing experimental plots on lake islands in northern Sweden, in which
mosses, ericaceous dwarf-shrubs, and tree roots have been continually excluded from plots in
various combinations since 1996 (Wardle and Zackrisson 2005). (c, d) Experimental plots on
peatland in northern England, where mosses, ericaceous dwarf-shrubs (c), and graminoids (d)
have been removed from plots in various combinations (Ward et al. 2009). Images: (a, b) D.A.
Wardle; (c, d) R.D. Bardgett.

strongest effects. However, functional group removals frequently had very weak
effects on soil processes, because the remaining functional groups often compensated
for the effects of those functional groups that were removed. As discussed in Chapter 3,
Suding et al. (2008) also used species removals in combination with nutrient add-
itions to show that the slow-growing forb Geum rossii promoted soil microbial
176 • 5 Consequences of species losses and gains

feedbacks that slowed rates of nitrogen cycling, while the fast-growing grass
Deschampsia caespitosa promoted microbial feedbacks that enhanced nitrogen cyc-
ling. Further, in a peatland in northern England, Ward et al. (2009) used a removal
experiment coupled with [13C]CO2 pulse labelling to demonstrate that losses of plant
functional groups, notably ericaceous shrubs, can greatly increase total ecosystem
CO2 fluxes. Meanwhile, an ongoing removal experiment initiated in 1996 on forested
lake islands in northern Sweden (Wardle and Zackrisson 2005; Wardle et al. 2008a;
Fig. 5.6) revealed that losses of particular functional groups (notably ericaceous
dwarf shrubs) and species (notably Vaccinium myrtillus and Vaccinium vitis-idaea)
significantly impaired several belowground properties and promoted growth of
planted seedlings, but only on productive islands with relatively fertile soil.
In contrast, vascular plant removal treatments impaired nitrogen fixation by cyano-
bacteria living in feather mosses (the main source of nitrogen input to these ecosys-
tems) only on small and unproductive islands (Gundale et al. 2010). These types of
removal studies point to potentially important ecosystem-level consequences of plant
species and functional groups (as well as the loss of these plants from the ecosystem),
and emphasize the key role of plant functional traits in driving aboveground and
belowground processes, as also highlighted in Chapter 3.
Removal experiments are especially useful for understanding the effects of loss
of dominant species in forested ecosystems. The lengthy life span of most tree
species combined with their large size creates particular logistic difficulties in using
them for conventional species-richness/ecosystem-functioning experiments. Several
approaches have been applied to study the ecosystem effects of forest tree diversity
(Díaz et al. 2009), but most of these are able to address the issue only indirectly.
However, there are many instances worldwide in which forests have been selectively
logged and from which particular tree species have been removed, and comparisons of
selectively logged stands with those that have not been logged serve as unintended
removal experiments experiments for investigating the ecosystem consequences of
losses of particular tree species (Díaz et al. 2003). Using such an approach, Wardle
et al. (2008c) studied the aboveground and belowground consequences of loss of a
highly desirable timber tree species, namely the podocarp Dacrydium cupressinum,
through selective logging in New Zealand rainforest, approximately 40 years after the
logging had been performed. This tree species has contrasting functional traits (e.g.
litter quality) to those of the other dominant tree species present in these forests, and
loss of this species was found to cause important effects on understorey vegetation,
soil carbon sequestration, soil nutrients, and the structure of the soil microbial com-
munity. The ecosystem-level effects of selective loss of a tree species from a forest
will, however, be case-specific and depend upon the differences in traits between those
species that are lost and not lost (Díaz et al. 2009), and possibly the sequence of species
loss (Bunker et al. 2005). In any case, measurements performed on selectively logged
forests may have considerable potential for understanding the consequences of losses
of long-lived species from an ecosystem arising from direct human intervention.
With regard to belowground biota, it is not possible to determine the extent to
which many groups of soil organisms are being subjected to extinction, even on local
 a a
120 a a a a a a
a a
(mg CO2–C g–1 h–1)
Basal respiration b bc b
b b bc c b b
b c c
80 b c

40

0
–R+R –R+R –R+R –S+S –S+S –S+S –M+M –M+M –M+M –V+V –V+V –V+V
Substrate-induced respiraton

500 a
a a
(mg CO2–C g–1 h–1)

a ab a a a a
b ab ab bc b b
c cd b b b b
c d d
250

0
–R+R –R+R –R+R –S+S –S+S –S+S –M+M –M+M –M+M –V+V –V+V –V+V

100
Total mineral nitrogen

a
a a
a a b ab b
b b bc
b b c bc
(mg g–1)

b c
c c c c c c c
10

1
–R+R –R+R –R+R –S+S –S+S –S+S –M+M –M+M –M+M –V+V –V+V –V+V
(mineral N)/(mineral N + DON)

0.8
a
ab a a
bc b a a
c
Ratio

ab
0.4 c c b b b
a a
a a
a b b b
b

0
–R+R –R+R –R+R –S+S –S+S –S+S –M+M –M+M –M+M –V+V –V+V –V+V

50 a a
a a a
b b a
bc bc b b
Decomposition

b bc
bc c c
(% mass loss)

c c c c c c c

25

0
–R+R –R+R –R+R –S+S –S+S –S+S –M+M –M+M –M+M –V+V –V+V –V+V
Medium

Medium

Medium

Medium
islands

islands

islands

islands

islands

islands

islands

islands
islands

islands

islands

islands
Large

Large

Large

Large
Small

Small

Small

Small

Fig. 5.6 Interactive effects of island size and removals of functional groups or species on selected
belowground properties after 7 years of an ongoing plant-removal experiment. Removal treatments
shown are: tree roots removed (R) or not removed (þR); all shrubs removed (S) or not
removed (þS); Vaccinium myrtillus removed (M) or not removed (þM); and Vaccinium vitis-
idaea removed (V) or not removed (þV). DON, dissolved organic nitrogen. Within each panel,
bars topped by the same letter are not significantly different at P ¼ 0.05 (least significant difference
(LSD) test), and vertical bars represent LSD values at P ¼ 0.05. From Wardle and Zackrisson (2005),
with permission from Macmillan Publishers Ltd.
178 • 5 Consequences of species losses and gains

scales. This is especially the case for groups such as bacteria, fungi, protozoa, and
some components of the nematode fauna, which may often not be greatly dispersal
limited (Finlay 2002), and for which over 90% of species remain unknown or under-
described (Klopatek et al. 1992; Coleman and Crossley 1995). Nevertheless, insights
into the ecosystem-level consequences of losses of subsets of the soil microbial
community have been achieved through removal of subsets of the microbial com-
munity through experimental perturbations. For example, fumigation of soil has been
shown by Degens (1998) and Griffiths et al. (2000) to cause detectable shifts in
microbial community composition and reductions of microbial diversity. In both of
these studies, such shifts impacted on processes driven by the decomposer commu-
nity, and in the case of Griffiths et al. (2000) they reduced the resistance of the
microbial community to a second stress, namely copper addition. Similarly, serial
dilution of soil results in progressive loss of microbial diversity, and on statistical
grounds it is expected that those taxa which are least abundant should be lost first.
However, the reduction of microbial diversity through dilution has been shown to
have little effect on rates of key soil processes driven by the decomposer community
and their stability (Griffiths et al. 2001), or on the resistance or resilience of processes
driven by denitrifiers and nitrate oxidizers (Wertz et al. 2007). This suggests that
those species removed from the microbial community by dilution are either func-
tionally replaceable or unimportant. Other studies have shown that the application of
toxic substances to soil, such as heavy metals, can selectively remove subsets of the
microbial community, and thereby impair ecosystem processes. For example, heavy
metal application can reduce the diversity of rhizobial strains, including those strains
that are most effective at fixing atmospheric nitrogen, and therefore impair symbiotic
nitrogen fixation (Giller et al. 1998).
Groups of soil fauna with larger body sizes are more amendable to study by
removal or exclusion approaches, at least at the functional group level. For example,
meshes with different hole sizes have been used to selectively exclude soil animals on
the basis of body size; studies using this approach show that animal body-size
distribution plays a role in affecting both decomposer processes (Vossbrink et al.
1979; Wardle et al. 2003c) and plant growth (Setälä et al. 1996). Selective biocides
have also widely been used as a tool, at least historically (Santos et al. 1981; Ingham
et al. 1986; Beare et al. 1992; Heneghan et al. 1999), for quantifying the effect that
different subsets of the soil faunal community may exert on other components of the
decomposer subsystem. Such studies have significantly advanced our understanding
about how loss of certain soil groups alters ecosystem functioning, although they also
have limitations in that the biocide may also exert side effects on the ecosystem
response variable of interest. Removal of larger-bodied soil organisms is also pos-
sible using other approaches. For example, removal of earthworms has been per-
formed by ‘electroshocking’ the soil, which drives most of the earthworms to the soil
surface (from where they can then be collected) while keeping other soil properties
and organisms intact (Bohlen et al. 1995; Staddon et al. 2003). Larger surface-
dwelling predators can also be kept out of study plots by appropriately designed
exclusion fences; as discussed in Chapter 2, these have been used to quantify the
 5.2 Species losses through extinction • 179

indirect effects of predatory spiders (Kajak et al. 1993; Lensing and Wise 2006) and
salamanders (Wyman 1998) on plant litter decomposition through their influence on
detritivores. In sum, removal approaches applied to the soil faunal community offer
important insights about the effects of losses of specific functional groups of soil
fauna (or subsets of the faunal community with particular functional attributes) on the
decomposer subsystem, and consistently point to impairment of ecosystem processes
when these organisms are lost.
As highlighted in Chapter 4, aboveground herbivores operate as important eco-
system drivers both aboveground and belowground, and this has been shown through
a large number of studies that have taken a removal or exclusion approach. For
example, several studies have used insecticides to illustrate the importance of inver-
tebrate herbivory in influencing plant community structure (Siemann et al. 2003), and
the indirect consequences of this for groups of soil organisms (e.g. Brown and Gange
1989, 1990) and decomposer-driven soil processes (e.g. Mulder et al. 1999). How-
ever, as mentioned above, one problem with such studies involves non-target effects
of the insecticide on the response variables of interest (Siemann et al. 2003). The
aboveground and belowground effects of larger bodied herbivores (i.e. vertebrates)
have been very commonly investigated through removal experiments that involve
the use of fenced exclusion plots. Studies that have used this approach for this
purpose have been discussed extensively in Chapter 4 and so will not be reviewed
in depth here. However, in the context of this discussion, we emphasize that
fenced exclusion studies are very useful both for predicting the effects of losses
of large herbivores that may occur through local extinction, and for determining
the effects of re-introduction of locally extinct herbivores, such as was used to
study the consequences of re-introduction of bison (Bison bison) into tallgrass
prairies in Kansas, USA (Knapp et al. 1999). Exclosure studies also lend themselves
to selective removal of vertebrate herbivores based on body size, through the use of
fences with different hole size or height (e.g. Bakker et al. 2004, 2006). Such studies
potentially offer insights into the ecological effects of losing some vertebrate species
(e.g. large-bodied ones) while retaining others, and also enable determination of how
the loss of some herbivores might influence the ecosystem impact of others that remain
(Bakker et al. 2004).
It is apparent from the above discussion that removal experiments have been
applied to a diverse range of taxa and ecosystems to understand what happens
when species or groups of species are lost from real ecosystems. Despite this, the
extent to which effects of species losses are influenced by species attributes and how
they vary across ecosystems remains relatively little understood. However, as dis-
cussed above, there is some evidence from the studies of Wardle and Zackrisson
(2005), Wardle et al. (2008a), and Gundale et al. (2010) that whether and how losses
of forest understorey species affect belowground properties and feedbacks depends
on soil fertility and ecosystem productivity (Fig. 5.6), which points to the role of
environmental context in governing whether and how species losses affect ecosystem
functioning. Such findings suggest that the nature of ecosystem-level responses to the
loss of a particular species resulting from human activity could differ greatly among
180 • 5 Consequences of species losses and gains

contrasting ecosystems. If this is the case, then an improved understanding of the

effects of species removal on ecosystem properties may be achieved by an increased
focus on how ecosystem properties and species attributes (i.e. traits) determine the
ecosystem-level consequences of species loss.

5.2.3 Effects of species losses in real ecosystems

As discussed so far in this chapter, there has been a tremendous amount of activity
directed to understanding how biodiversity affects ecosystem functioning, and a
range of approaches have been used, from large-scale, observational studies to highly
controlled experimental studies (Díaz et al. 2003). These approaches vary greatly in
their applicability for understanding how species losses affect ecosystem-level prop-
erties in the real world. As such, it is important to note that the question of how
species richness affects ecosystem functioning is different to that of how species
losses during real extinction events affect ecosystem functioning, and different
approaches may be best suited for each of the two questions (Fig. 5.7). Although
random assembly experiments have been the most widely used approach for explor-
ing how biodiversity losses affect ecosystem functioning, they are only relevant to
this question if it is assumed that ecological communities are randomly assembled
and if species from that community are lost at random (i.e. independent of species
attributes) during extinction. As discussed earlier, whenever species traits that pre-
dispose a species to extinction are the same as those that are important for driving
ecosystem functioning, then the effects of species loss are likely to be much greater
than would be predicted through random assembly experiments. It is likely that this is
frequently the case, and there is evidence for this from empirical (Petchey et al. 1999;
Jonsson et al. 2002; Zavaleta and Hulvey 2004) and theoretical (Solan et al. 2004;
Bunker et al. 2005) studies. As such, random assembly experiments may greatly

Loss of species in Experiments involving Experiments with

real ecosystems non-random removal random assemblages of
through human of species from real species with differing
activity ecosystems richness

Control by experimenter

Relevance to understanding effects of species richness

Relevance to understanding effects of species extinctions

Fig. 5.7 Approaches that have been used to address the issue of how biodiversity losses
(i.e. extinctions) through human activity may influence the functioning of ecosystems.
 5.2 Species losses through extinction • 181

underestimate effects of species losses on ecosystem properties, and despite strong

assertions to the contrary (e.g. Duffy 2009) this diminishes the relevance of such
experiments for understanding the ecosystem effects of species losses (Wardle and
Jonsson 2010).
Determination of how species losses through human activity may affect
ecosystem processes is arguably most realistically and directly studied by meas-
uring how the ecosystem responds to the actual species losses that have occurred.
This is analogous to the large number of studies that have directly assessed how
ecosystems respond to the gain of new species through biological invasion, an
approach that has frequently proven its worth and advanced our understanding
about invasion ecology, as discussed later in this chapter. With regard to plant
communities, few studies have directly quantified the effects of actual species
losses resulting from human activity. Those that have been done so far have
focused largely on the selective removal of tree species that have occurred through
logging as discussed above, and such studies have shown that these losses can
have particularly important consequences for ecosystem functioning when the
harvested species are the structural dominants of the forest (Díaz et al. 2003;
Wardle et al. 2008c). Natural or unintended ‘removal experiments’ of this type
arguably represent the most direct means available for assessing the effects of real
species losses in ecosystems resulting from human-induced alterations of either
abiotic or biotic environmental conditions.
Some of the most convincing studies of how actual losses of species affect
ecological processes involve situations in which aboveground mammal species
have become locally extinct. As outlined in Chapter 4, herbivorous mammals and
their predators often have major effects on ecosystem processes, meaning that the loss
of these species is also likely to have important consequences. For example, the North
American bison (Bison bison), which was once the dominant mega-herbivore of the
North American Great Plains, was reduced to a few thousand individuals by the
1880s and had become extinct from much of its natural range. Re-introduction of
bison to the Konza Prairie in the mid-1980s, together with the use of fenced plots
from which reintroduced bison were excluded, provides evidence that the loss of
bison causes altered floristic composition and reduced plant diversity, reduced spatial
variability of vegetation, reduced rates of soil nitrogen mineralization, and reduced
plant-tissue nitrogen concentrations (Knapp et al. 1999; Johnson and Matchett 2001).
Further, the loss of large predators, such as has occurred in many ecosystems
worldwide due to human activity, can set a cascade in motion through causing
population growth (and overabundance) of herbivorous prey (Wardle and Bardgett
2004). For example, the loss of the cougar (Pumus concolor) and wolf (Canis lupus)
in many natural ecosystems in North America has led to large increases in cervid
species (white-tailed deer (Odocoileus virginianus), elk (Cervus canadensis), and
moose (Alces alces)). These increases have been shown to alter consumption by
cervids of palatable plant species (Creel and Christianson 2009), greatly alter forest
vegetation composition (Ripple and Beschta 2008), reduce understorey and riparian
vegetation, promote erosion, and alter the hydrology of whole watersheds (Ripple
182 • 5 Consequences of species losses and gains

and Betscha 2006; Betshsa and Ripple 2008). Given the impact of mammalian
herbivores on nutrient cycling, as considered in Chapter 4, it is likely that losses of
their predators would also exacerbate these effects. For example, studies on the
reintroduction of wolves into Yellowstone National Park (Frank 2008) provide
evidence that the loss of wolves and resulting increases in ungulate densities in
turn indirectly promote soil nitrogen mineralization and presumably the soil organ-
isms that drive this process.
The effect of loss of large mammals on the present-day functioning of ecosystems
is also apparent through extinctions that occurred hundreds to thousands of years ago.
Human colonization of new regions has often coincided with the extinction of mega-
herbivore species, although there is some uncertainty about the extent to which these
extinctions have been caused directly by humans or by other factors such as climate
and vegetation change (Zimov et al. 1995; Guthrie 2003). Nevertheless, there is
evidence that mega-herbivore extinction is likely to have caused major shifts in the
types of vascular plants present and the functioning of the belowground subsystem.
For example, it has been proposed that the extinction of mega-herbivores in Alaska
and Russia over the past 10 000–12 000 years has led to a shift from grazed steppe
grassland to wet moss-dominated tundra (Zimov et al. 1995). This has led to
domination by plant species that produce poorer-quality litter, greater water-logging,
and impairment of soil nitrogen mineralization, setting a feedback in motion that
maintains domination by tundra vegetation (Fig. 5.8). Wherever human colonization
has been associated with losses of mega-herbivore species, there are likely to have
been large and irreversible consequences for aboveground–belowground linkages
and therefore the functioning of the ecosystem.
Before leaving the topic of how species losses impact on ecosystem functioning,
we highlight that the most widely documented and convincing examples involve
ecosystem impacts of losses of large organisms, such as trees and some mammal
species. As a result of their large size, they are both more likely to be utilized by
humans for resources (e.g. trees and herbivorous mammals) or deliberately exter-
minated (e.g. large predators), and to have disproportionate effects on the functioning

Dry soils High evapo- Moist soils Low evapo-

transpiration transpiration
High soil oxygen Low soil oxygen

Mega-
High mineralization rates Low mineralization rates
herbivores

High nutrient Faeces, MEGA- Low nutrient

availability urine HERBIVORE availability
High EXTINCTION
litter Low
quality PRODUCTIVE Surface litter UNPRODUCTIVE Low surface
STEPPE disturbance quality TUNDRA disturbance

Fig. 5.8 Effects of mega-herbivore extinction in northern Russia in the late Pleistocene on
feedbacks between vegetation and nutrient cycling, as hypothesized by Zimov et al. (1995).
From Wardle, David A. ‘Communities and Ecosystems’ Ó (2002), Princeton University Press,
reprinted by permission from Princeton University Press.
 5.3 Species gains through invasion • 183

of the ecosystem. There are few examples of human-induced losses of smaller bodied
organisms, including soil organisms, impacting on community and ecosystem pro-
cesses. This may be because losses of smaller-bodied species often have smaller
effects on ecosystem properties, or because when smaller organisms are lost their
ecological impact (and even the fact that the species has been lost) is less likely to be
detected.

5.3 Species gains through invasion and aboveground–

belowground linkages
Ingress of alien (including invasive) organisms into a new ecosystem is to some
extent the reverse of extinction, as it results in the gain of novel species by a
community. As is the case for extinction, invasive species are most likely to exert
important community and ecosystem-level effects when they become biomass dom-
inants within their trophic level, or have traits that differ greatly from those of the
native species. There has been much research activity, and significant recent concep-
tual advances, in understanding the impacts of the ingress of new species into
biological communities, which we now discuss.

5.3.1 Invasions by plants

5.3.1.1 Functional Differences between Invasive and Native Species
The majority of studies that have considered invasive species from a combined
aboveground–belowground perspective involve invasive plants. In plant communi-
ties, most alien species become minor and functionally unimportant components of
the invaded community (Thompson et al. 1995), but a subset of species do have major
effects on the functioning of ecosystems due to key trait differences. In this light,
studies that have compared native and alien components of floras have often found
significant differences in key functional traits between the two groups. For example,
Baruch and Goldstein (1999) found that for 63 plant species in the Hawai’ian
archipelago, invasive species as a group had leaf traits linked to greater resource
capture (i.e. high specific leaf areas, carbon dioxide assimilation rates, and concen-
trations of foliar nutrients) relative to native species (Fig. 5.9). Similarly, Leishman
et al. (2007) and Peltzer et al. (2009) have found, for floras near Sydney, Australia,
and Kaikoura, New Zealand, respectively, that alien species on average had higher
specific leaf areas and nitrogen and phosphorus concentrations than did native species
(Fig. 5.9). However, differences in leaf traits between invasive and native species
may depend greatly upon habitat conditions (Baruch and Goldstein 1999). For
example, Funk and Vitousek (2007) found, through comparing pairs of phylogenet-
ically related plant species in Hawai’i, that alien plant species on average had greater
photosynthetic rates and resource (i.e. water, nutrient, and light) use efficiencies than
did native species. However, they also found that several of these differences were
mostly apparent only over short timescales and were strongly dependent upon the
184 • 5 Consequences of species losses and gains

250

200
SLA (cm–2 g–1)

150

100

50

3.0

2.5

2.0
N (%)

1.5

1.0

0.5

0.0

0.20

0.15
P (%)

0.10

0.05

0.00
Invasive Native Invasive Native Invasive Native
Hawai’i Australia New Zealand

Fig. 5.9 Comparison of specific leaf area (SLA) and leaf nitrogen (N) and phosphorus (P)
concentrations between native and exotic components of floras along an elevational gradient in
Hawai’i (64 species; Baruch and Goldstein 1999), in bushland near Sydney, Australia (55
species; Leishman et al. 2007), and on a river floodplain near Kaikoura, New Zealand (41
species; Peltzer et al. 2009).

nature of resource limitation in the habitat in which they were growing. Nevertheless,
evidence to date does generally point to native and alien species showing overall and
consistent differences in key ecophysiological traits (Rejmanek et al. 2005).
The key traits that often differ between native and alien species are well known to
control litter-decomposition processes, as discussed in Chapter 3. For this reason, it is
 5.3 Species gains through invasion • 185

expected that decomposability of litter should differ between the two types of plants,
although few studies have performed comparative studies on rates of litter decom-
position of large numbers of native and invasive species. A meta-analysis of 94
studies by Liao et al. (2008) showed that on average litter from invasive species
decomposed 2.17 times faster than that from non-invasive species, although this
effect diminishes when nitrogen-fixing plant species are not included in the analyses.
Further, in that analysis it is difficult to ascertain whether or not this difference was
mostly due to phylogenetic differences between the two groups. Meanwhile, Allison
and Vitousek (2004) compared litter-decomposition rates for 11 understorey Hawai’ian
plant species (five native and six invasive) and found that litter from the natives did
decompose more slowly. However, all but one of the natives were ferns and all but
one of the invaders were angiosperms, and it is recognized that fern litter usually
decomposes more slowly than that from angiosperms (see Chapter 3). Meanwhile,
Kurokawa et al. (2010) compared rates of litter decomposition for 41 New Zealand
riverplain shrub species, and found, that as a group, litter from invasive nitrogen-
fixing species decomposed faster than that from native nitrogen fixers. However,
there was no difference in litter decomposability between native and exotic non-
nitrogen fixers. Other studies that have compared rates of litter decomposition for
smaller numbers of coexisting native and invasive species (reviewed by Ehrenfeld
2003) have often found litters of invaders to decompose more rapidly (e.g. Cameron
and Spencer 1989; Standish et al. 2004), although there are many exceptions (e.g.
Kourtev et al. 2002b; Güsewell et al. 2006), especially when the native and invasive
species have different life forms. For example, exotic pine tree species, a major
invasive problem in many ecosystems worldwide (Richardson 2006), are often likely
to produce litters that decompose more slowly than those produced by the native
species (Ågren and Knecht 2001; Ehrenfeld 2003) (Fig. 5.10).
Functional differences between coexisting invasive and non-invasive species also
have consequences belowground. The most substantial effects of invaders often arise
when the invader is able to form nodules that fix atmospheric nitrogen while the
native species cannot. In a classic study, Vitousek and Walker (1989) found that the
invasion of the actinorhizal shrub Myrica faya (native to the Azores and Canary
Islands) into a montane forest site in Hawai’i, which lacked nitrogen-fixing plant
species, led to an over four-fold increase in ecosystem nitrogen input. This should in
turn have large ecosystem-level consequences through alleviating nitrogen limitation
at the site. However, non-nitrogen-fixing invasive species also cause important
changes in soil properties, and often (though not always) promote nutrient flux
rates (Ehrenfeld 2003) and the availability of plant-available nitrogen (Zou et al.
2006), phosphorus (Chapuis-Lardy et al. 2006), and other minerals (Vanderhoeven
et al. 2005). As a result of alteration of the quality and quantity of resources entering
the soil, invasive plants also cause profound changes in soil food webs. For example,
Kourtev et al. (2002a) found that invasive understorey plant species in forests in New
Jersey, USA, exerted substantial effects on the composition of the soil microbial
community. Further, populations of soil fauna (nematodes and microarthropods) in
grasslands in south-eastern Utah have been shown to respond negatively to invasion
186 • 5 Consequences of species losses and gains

(a)

(b)

Fig. 5.10 Invasive Pinus contorta trees, native to North America, invading grassland in the
Craigieburn range of New Zealand. Invasive pine trees produce poor-quality litter and acidify
soils, leading to impairment of belowground processes and alteration of the belowground
community. Image by D. Peltzer.

by the exotic grass Bromus tectorum (Belnap et al. 2005). Similarly, Yeates and
Williams (2001) found invasion of native ecosystems by each of three exotic plant
species in New Zealand to influence soil microfaunal communities, although the
extent of these effects depended on both the plant species and location. Belowground
 5.3 Species gains through invasion • 187

impacts of invasive plants may be apparent even when the invaders do not dominate
the plant biomass, especially if they have sufficiently distinct functional character-
istics. For example, Peltzer et al. (2009) showed that for a New Zealand floodplain
community, non-native species exerted disproportionate effects on the soil microbial
community and on microbe-feeding and predatory nematodes, despite occupying
only 3% of the standing plant biomass (Fig. 3.10).
Invasive plants can also potentially exert important effects both aboveground and
belowground by altering the disturbance regime of the ecosystem (Mack and
D’Antonio 1998). This is especially apparent when invasive and native species differ
in key traits that affect their relative flammability, because this has important conse-
quences for the ecosystem’s fire regime. Notably, invasive grasses that invade woody
ecosystems in Hawai’i, Australia, and North and South America produce highly
flammable tissues and greatly increase the fuel load for fires at the ground layer,
leading to an increased occurrence of fires in these ecosystem (Brooks et al. 2004;
Bradley et al. 2006; Pauchard et al. 2008). For example, in Hawai’i, invasion of
perennial C4 grasses into sub-montane forest results in rapid accumulation of highly
flammable material, resulting in fires that kill most of the natural vegetation. The
grasses recover rapidly after fire while the native species do not, setting in motion a
positive feedback between fire and the exotic grasses (D’Antonio and Vitousek 1992;
Brooks et al. 2004). Given that fire exerts a multitude of effects on the belowground
subsystem (Certini 2005), it is inevitable that invader-induced shifts in fire regime
would have important belowground consequences, although these have seldom been
addressed. However, Ley and D’Antonio (1998) found in Hawai’i that rates of
nitrogen fixation were greater in fire-driven grassland dominated by alien grasses
than in adjacent uninvaded woodland. This was because the main substrate upon
which the nitrogen fixation occurs, namely leaf litter from native woody species, is
largely absent from the grassland.

5.3.1.2 Invasive Plant Species and Plant–Soil Feedbacks

Differential effects of native and invasive plant species on soil biota can in turn have
important feedback effects on plant performance. As discussed in Chapter 3 (see also
Fig. 3.11), a large number of recent studies have experimentally investigated feed-
backs between plants and soil organisms. One significant application of this approach
has been the study of relationships between invasive plant species and their associ-
ated soil biota (see reviews by Wolfe and Klironomos 2005; Van der Putten et al.
2007). In a landmark study, Klironomos (2002) utilized plant–soil feedback experi-
ments to show that invasive plant species in Canadian grassland and meadow
ecosystems consistently showed positive plant–soil feedbacks, while rare native
plant species consistently showed negative feedbacks (Fig. 5.11). This work indicates
that invasive species may derive a benefit from entering positive feedbacks with
their soil biota in their new habitat. As evidence for this, feedback experiments have
since been used to provide evidence that invasive species respond more favourably
(or less unfavourably) to their soil biota in their new habitat than in their native range
188 • 5 Consequences of species losses and gains

0.6
0.5
0.4
Growth of plants with their own soil relative

0.3
to that with soil from other species

0.2
0.1
0
–0.1
–0.2
–0.3
–0.4
–0.5
–0.6
–0.7
–0.8

Liatris

Aletris
Alliara

Cirsium
Lythrum

Agalinis
Polygala
Gentiana
Euphorbia

Polygonum

Invasive Rare

Fig. 5.11 The results of a soil-feedback experiment for five invasive and five rare native plant
species from Canadian grasslands and meadows. Bars represent the mean + 1 SE (n ¼ 10).
Note that invasive plants undergo positive feedbacks with their associated soil biota, while rare
species undergo negative feedbacks. Modified from Klironomos (2002), with permission from
Macmillan Publishers Ltd.

(e.g. Reinhart et al. 2003; Callaway et al. 2004; Knevel et al. 2004). For example,
Reinhart et al. (2003) used feedback experiments to show that black cherry (Prunus
serotina) was negatively influenced by the soil community that developed under it in
its native range in North America, while it was positively influenced by its soil
community in its new range in north-western Europe. Such studies provide evidence
that invasive plant species may perform better in their new range through escaping
soil antagonists (e.g. pathogens) that regulate their populations in their native range,
supporting the enemy release hypothesis (Elton 1958; Keane and Crawley 2002).
However, some caution is needed in interpreting the results of such experiments,
because few studies (but see Reinhart et al. 2003) have utilized both soils and plants
from both native and non-native ranges, which is an important requirement for
providing convincing evidence of this hypothesis (Van der Putten et al. 2007).
The belowground effects of invasive plant species can also have important conse-
quences for coexisting native species. One route by which this may occur is through
invading plant species releasing allelochemical compounds that in turn impact
 5.3 Species gains through invasion • 189

negatively on native plant species (Wardle et al. 1998b, Ridenour and Callaway
2001). A development of this idea is the so-called novel weapons hypothesis which
proposes that invasive plant species can release phytotoxic compounds to the soil that
are novel to the native plant species and to which the native species are non-adapted
and therefore vulnerable (Callaway and Ridenour 2004). There are several claims in
the literature of species invading new communities in turn exerting phytotoxic effects
against the resident species, although there are difficulties in providing unequivocal
evidence of these effects (Harper 1977; Stowe 1979; Keeley 1988). One example that
has gained much attention is the ability of the invasive Eurasian plant Centaurea
maculosa (spotted knapweed) to produce ()-catechin, which reportedly has a
greater adverse effects on grass species in its invasive range (i.e. in North America)
than on related grass species in its native range (e.g. Bais et al. 2003; Callaway and
Ridenour 2004; Thorpe et al. 2009). However, subsequent investigations have
suggested that ()-catechin released from C. maculosa may not reach sufficient
concentrations in the soil to exert negative effects on its neighbours (Blair et al.
2005; Perry et al. 2007; Duke et al. 2009). Other studies have presented evidence that
invasive plant species may adversely affect coexisting species by disrupting their
mycorrhizal symbionts. This has recently been shown for the invasive non-mycor-
rhizal plant Alliaria petiolata (garlic mustard), which adversely affects ectomycor-
rhizal fungi associated with seedlings of coexisting native species when it invades
forests in North America (Stinson et al. 2006; Callaway et al. 2008; Wolfe et al.
2008). It has been proposed that mycotoxoins (‘novel weapons’) produced by A.
petiolata are responsible for its effects in the habitats that it invades in each of these
studies. However, as with ()-catechin, it is unknown whether these toxins actually
accumulate in soils in the invaded areas in sufficient concentrations to exert these
effects.
Although many studies have focused on the success of invasive plant species in
new habitats through escaping their belowground enemies, plants invading new
habitats can also leave behind their belowground mutualists which could impair
their success. This is likely to be important for invasive plant species that rely on
ectomycorrhizal fungal mutualists, such as pine trees in much of the Southern
Hemisphere (Richardson et al. 1994, 2000). Here, pine species often invade native
communities that lack ectomycorrhizal hosts, and rapid invasion of pines may
therefore occur only after arrival of windborne ectomycorrhizal fungal spores, for
example from nearby pine plantations where the trees have been deliberately inocu-
lated (Richardson et al. 2000; Nuñez et al. 2009). In contrast, invasive plants that
form arbuscular mycorrhizal associations are usually less likely to be impaired by the
availability of fungal inocula, because arbuscular mycorrhizal fungi are very widely
distributed and have lower host specificity (Richardson et al. 2000). In the case of
invasive plants that form mutualistic symbioses with nitrogen-fixing bacteria (i.e.
Rhizobium and Frankia), the bacterial symbionts are often widespread even in soils
that lack hosts, and the deliberate introduction of bacterial symbionts to many regions
worldwide contributes to the success of these plants as invaders (Richardson et al.
2000; Van der Putten et al. 2007). In some cases, it is unclear as to where these
190 • 5 Consequences of species losses and gains

symbiotic bacteria arise from. For example, it is unknown whether the highly
successful actinorhizal invasive plant Myrica faya in Hawai’i (Vitousek and Walker
1989) arrived with its own strains of Frankia, or whether compatible strains of
Frankia were already present in the soil (Richardson et al. 2000). The most wide-
spread mutualism between plants and soil organisms is arguably between plants and
their associated saprophytes that mineralize nutrients required for plant growth (see
Chapter 3). Here, the saprophytic community consists of organisms that have a wide
range of functional capacities, and most soils contain most functional groups of
saprophytes. For this reason, it is highly unlikely that invasive plant species will
‘escape’ saprophytic microbes with particular functional capabilities in their old
environment or encounter new types of saprophytes in their new environment (Van
der Putten et al. 2007).
Before leaving the topic of invasive plants, it is important to stress that there are three
factors that collectively contribute to the total ecological impact of any invasive plant
species, namely, range, abundance, and per-capita or per-biomass effect of the invader
(Parker et al. 1999). As such, while most studies of the effects of invasive plants
belowground (and their feedback effects aboveground) have focused on the third of
these factors, the invader can only have important ecological impacts if it also occupies
a sufficient range and becomes abundant. The ability of a potential invader to increase
its range and abundance in a new habitat will be determined by the demographic and
physiological traits of the invader, and by the characteristics of the habitat and
plant community being invaded. As such, the extent to which a native plant community
can resist invasion will reduce the magnitude of the impact of the invader, both
aboveground and belowground. As a consequence, native plant community properties
and traits of the dominant plant species (Fridley et al. 2007), the nature of resource
supply and availability (Huston 1994; Davis et al. 2000), and disturbance regime
(Burke and Grime 1996) are all important determinants of whether, and how much,
the community is likely to be invaded in the first place. An improved understanding
of how invasive plant species can impact upon ecosystems will therefore gained
by considering not just the effect of the invader once it has become established, but
also whether the invader may increase its range and abundance sufficiently to exert
important effects in the first place.

5.3.2 Belowground invaders

In general, there is relatively little known about the occurrence or ecological signifi-
cance of invasive microorganisms. However, as discussed earlier in this chapter,
many groups of saprophytic microbes may not be dispersal-limited at a global scale
(Finlay 2002), thereby reducing the scope for microbes to invade new habitats.
However, were invasions of species of saprophytic microbes to occur, they would
likely remain undetected because most saprophytes have not been described at the
species level (Van der Putten et al. 2007). Further, given the considerable functional
diversity of the microbial saprophytic community, it is unlikely that an invasive
microbe would possess sufficiently novel functional attributes for its ecological
 5.3 Species gains through invasion • 191

effects to become detected. However, there are some well-documented examples of

pathogenic soil-borne fungi invading new habitats and causing widespread effects on
vegetation in native ecosystems (reviewed by Desprez-Loustau et al. 2007; Loo
2009). For example, dieback of natural vegetation in Australia has resulted from
invasion by the root pathogenic fungi such as Phytophthora cinnamomi (Peters and
Weste 1997) and Armillaria luteobubalina (Shearer et al. 1998). Similarly, in
California, invasion by Phytophthora ramorum is well known to influence a range
of vascular plant species and cause sudden oak death syndrome (Venette and Cohen
2006). Such examples point to invasive pathogens having novel modes of attack that
the native flora is poorly adapted to withstand. There are also examples of invasive
mutualistic fungi that form associations with native tree species. For example, the
distinctive European ectomycorrhizal fungus Amanita muscaria has invaded native
forests in New Zealand and Australia (Fig. 5.12), while Amanita phalloides has
spread from Europe to forested ecosystems elsewhere around the world (Pringle
and Vellinga 2006). However, the impact of invasive ectomycorrhizal fungi on native
tree growth, the native ectomycorrhizal community, or the decomposer subsystem
remains little understood.
With regard to belowground invertebrates, little is known about invasions in
natural ecosystems involving microfauna, such as nematodes and protozoa, largely
because the vast majority of species have not been described. Further, it is possible

Fig. 5.12 The well known ectomycorrhizal fungus Amanita muscaria or fly agaric, native to
Europe, is a distinctive invader of native forests in New Zealand and Australia, where it forms
associations with native tree species. However, the impact of invasion by this fungus on native
tree growth, the native ectomycorrhizal fungal community, or other components of the
ecosystem, remains little understood. Image by Ian Dickie.
192 • 5 Consequences of species losses and gains

that, like microbes, at least a subset of the soil microfaunal community may not be
dispersal-limited at global scales (Finlay 2002; but see Foissner et al. 2008). How-
ever, larger-bodied soil invertebrates that are constrained by biogeographical bound-
aries are certainly capable of invading new ecosystems. With regard to mesofauna,
some of the best-documented examples involve invasion of sub-Antarctic islands by
European species of Collembola (Frenot et al. 2005). For example, invasive collem-
bolan species can reach very high densities on sub-Antarctic Marion Island, and it has
been suggested that this could be causing displacement of native collembolan species
(Convey et al. 1999). Further, invasion of ecosystems by larger-bodied saprophagous
soil organisms, such as millipedes and isopods, and insects such as beetles and
dipterans that spend at least part of their life cycle belowground, are well documented
in many parts of the world (e.g. Gaston et al. 2003; Arndt and Perner 2008). However,
the effects of these invaders on native decomposer fauna, soil processes, and plant
growth and nutrition remain largely unexplored.
The one belowground faunal group for which the effects of invasive species have
been comparatively well studied are the earthworms (see reviews by Bohlen et al.
2004b; Hendrix et al. 2008). Novel earthworm species have been introduced to many
temperate and tropical regions worldwide (Hendrix et al. 2008), and their ecological
impacts are particularly apparent when they invade ecosystems that lack functionally
comparable species. As such, strong impacts of invasive earthworms have been
shown in regions that lack a native earthworm fauna through Pleistocene glaciations
eliminating previous earthworm species (Hendrix et al. 2008). The belowground
consequences of earthworm invasions can be wide-ranging (Bohlen et al. 2004b;
Fig. 5.13). For example, the geophagous South American earthworm Pontoscolex
corethurus has invaded many forested and agricultural regions throughout the trop-
ics, where it alters and sometimes greatly enhances soil compaction and thus reduces
soil porosity (Chauvel et al. 1999). This can in turn result in a compact soil crust that
potentially negatively impacts both on other soil organisms and plant growth (Lapied
and Lavelle 2003; Gonzalez et al. 2006). Meanwhile, the epigeic European earth-
worm Dendrobaena octaedra has invaded natural forests in Alberta, Canada, and this
has favoured domination by faster growing fungal species and reduced the abundance
of many taxa of mites (McLean and Parkinson 2000a, 2000b). Further, earthworm
invasion in temperate North American forests can strongly influence soil physical
structure, enhance mineralization of organic matter, and lead to loss of soil organic
mater and nutrients; these effects are, however, far more pronounced for burrowing
than epigeic earthworm species (Bohlen et al. 2004a; Hale et al. 2005). Stimulation
by invasive earthworms of organic matter mineralization can cause short-term im-
provements in plant nutrition and growth (Scheu and Parkinson 1994), but in the
longer term it leads to removal of the surface organic layer, adversely affecting plant
species that are adapted to thick forest floors (Gundale 2002; Frelich et al. 2006). As
such, earthworm invasion may induce loss of native herbs while promoting some
invasive plant species (Bohlen et al. 2004b), and impair seedling recruitment of some
forest tree species (Frelich et al. 2006; Hale et al. 2006). However, the nature of
effects of earthworm invasion on aboveground and belowground properties depends
 5.3 Species gains through invasion • 193

Dispersal Resource quantity Resource quality Soil factors

• source population • plant productivity • vegetation type • moisture hydrology
• natural expansion • soil organic matter • litter C:N ratio • texture, sand/silt/clay
• human activity • tannins, polyphenotics • acidity, base cations
• streams, rivers

Earthworm
invasion

Physical effects Biological effects

• burrowing and casting Geochemical effects • change in soil habitat
• litter removal • mixing soil layers • faster nutrient cycling
• soil aggregates • adsorption/desorption • less fungally-dominated
• porosity • mineral weathering • fewer mycorrhizae
• hydrology • change in minerology • change in rooting zone
• erosion • altered seedbed

Ecological consequences

Ecosystem properties Ecological communities

• C loss (short term) • plant invasions
• C stabilization (long term) • loss of native herbs
• N retention? • soil invertebrate community shifts
• P availability? • microbial community shifts
• tree nutrition?

Fig. 5.13 Conceptual model demonstrating the wide-ranging effects that invasive earthworm
species can exert in North American temperate forests that lack native earthworm faunas. From
Bohlen et al. (2004b), with permission from the Ecological Society of America.

on the functional attributes of the earthworm species involved, as well as the

properties of the ecosystem being invaded. Earthworm invasion of natural forested
ecosystems in many regions is comparatively recent, and the long-term consequences
of their effects for forest dynamics remains largely unknown (Bohlen et al. 2004b).
Invasive predators of belowground organisms may also exert important ecosys-
tem-level effects, at least in cases where they consume organisms that have a
functionally irreplaceable role in the ecosystem. One of the most convincing ex-
amples is the predatory New Zealand flatworm Arthurdendyus triangulata, which has
been accidentally introduced to the British Isles and Faroe Islands where it has
subsequently spread and reduced the density of lumbricid earthworms upon which
it preys (Boag and Yeates 2001), potentially altering the invaded ecosystem. For
example, the loss of earthworms due to flatworm invasion in Scottish grasslands
has been shown to adversely affect soil porosity and drainage, leading to greater
water-logging, greater dominance of vegetation by rushes, and reduced densities of
burrowing moles (Boag 2000) (Fig. 5.14). Another example is the introduction of the
house mouse to the sub-Antarctic islands (Smith et al. 2002; Angel et al. 2009), such
as Marion Island. Here, mice consume many taxa of invertebrates, including the
194 • 5 Consequences of species losses and gains

(a)

(b)

Fig. 5.14 (a) The predatory New Zealand flatworm (Arthurdendyus triangulate), which
invades grasslands in the British Isles and Faroe Islands, where it greatly reduces the density
of burrowing lumbricid earthworms upon which it preys, thus reversing the ecosystem level
impact of earthworms in these ecosystems. (b) Removal of earthworms by the flatworm leads
to large reductions in soil porosity and water drainage, leading to waterlogging and increasing
dominance by rushes (Juncus spp.). Images by B. Boag.

endemic flightless moth Pringleophags marioni which otherwise functions as the

main marofaunal detritivore. In this system, predation of this moth by mice has been
estimated to reduce litter processing by the moth by up to 40% (Crafford 1990),
potentially leading to greatly increased rates of peat accumulation on the island
(Smith and Steenkamp 1990). Ground-dwelling predatory insect groups that contain
invasive members, such as ants and carabid beetles, are also likely to feed heavily on
detritivorous fauna and thus affect the processes that they drive. However, while
these types of predators are well known to adversely affect related native predators
 5.3 Species gains through invasion • 195

(Gotelli and Arnett 2000; Niemelä et al. 1997; Snyder and Evans 2006), their impact
upon belowground organisms and the processes that they drive remains unexplored
(Kenis et al. 2009).

5.3.3 Invasions by aboveground consumers

As discussed in Chapter 4, aboveground primary consumers have wide-ranging
effects on both the aboveground and belowground subsystems. These effects are
particularly strong for invasive consumers, especially when they have escaped their
natural enemies and when the new host species are not adapted to the invader. As
such, there are several examples of major changes in forest ecosystems brought about
by the invasion of both aboveground fungal pathogens (Desprez-Loustau et al. 2007;
Loo 2009) and herbivorous insects (Liebhold et al. 1995; Kenis et al. 2009). As a
well-known example of an invasive pathogen, chestnut blight (Cryphonectria para-
sitica) from Asia has resulted in widespread loss of the American chestnut (Castanea
dentata) in forests of the eastern USA. Because chestnut produced tannin-rich wood
that was of lower quality than that of co-occurring hardwood species that replaced it,
it has been suggested that invasion by the blight will have greatly altered the
decomposer subsystem and nutrient cycling (Ellison et al. 2005; Kenis et al. 2009).
Although not experimentally tested, significant belowground effects are also likely to
have resulted from the selective removal of single tree species in mixed-species forest
by other invasive aboveground pathogens, such as the widespread loss of elm
(Ulmus) trees following invasion by the Dutch elm disease (Ophiostona spp.). With
regard to insect herbivores, severe defoliation of native oak (Quercus) species in
North America by the invasive gypsy moth (Lymantria dispar) during outbreak
events can have substantial belowground effects that may feedback aboveground
(Lovett et al. 2006). In particular, following outbreaks there is a large pulse of
nitrogen and labile carbon to the forest floor that results from insect faeces, dead
caterpillars, and unconsumed fallen foliage; much of this nitrogen is in turn immo-
bilized by soil microbes or incorporated into soil organic matter (Lovett and Ruesink
1995). Further, the hemlock woolly adelgid (Adelges tsugae; an aphid-like invader) is
currently causing widespread death of hemlock (Tsuga) species in the north-eastern
USA. As hemlock species produce much poorer-quality litter than do most tree
species that are likely to replace it, the resulting shift in tree species composition
will probably long-term impacts on the structure and functioning of the ecosystem
(Lovett et al. 2006).
Mammalian herbivores, for example deer, rabbits, and goats, have been introduced
to many parts of the world where they can have major impacts on natural ecosystems,
both above and below ground (Wardle et al. 2001; Vázquez 2002; Spear and Chown
2009). For example, several species of deer, and domestic goats (Capra aegagrus
hircus), were deliberately introduced to New Zealand between the 1770s and 1920s,
where they have caused widespread compositional change in the forest understorey
through removing broad-leaved, fast-growing dicotyledonous plant species and pro-
moting other unpalatable species. New Zealand lacks native browsing mammals, and
196 • 5 Consequences of species losses and gains

the native mega-herbivores (i.e. the moa birds), which were hunted to extinction a
few hundred years ago, probably had much smaller effects on the forest than the
introduced browsers currently do (McGlone and Clarkson 1993). Using long-term
deer exclusion plots located in forests throughout New Zealand, Wardle et al. (2001,
2002) showed that invasive deer and goats caused consistent reductions of those
understorey plant species which produce high-quality and readily decomposable
litter, and generally promoted those species that produce poor-quality litter. Also,
browsing mammals were found to have consistently negative effects on large-bodied
soil organisms (Fig. 5.15), probably through adverse physical disturbance effects
resulting from trampling (Wardle et al. 2001). However, most groups of small-bodied
soil organisms, including microflora and microfauna, showed idiosyncratic responses
to invasive browsers, with both positive and negative effects being detected depend-
ing on the location (Fig. 5.15). Ecosystem properties driven by soil biota, such as soil
carbon mineralization and carbon and nitrogen sequestration also showed context-
dependent responses. These varied responses emerged because browsers can exert
either positive or negative effects on decomposers depending on environmental
context, as discussed in Chapter 4.
Ecosystem impacts resulting from the physical effects of invasive herbivores may
be especially significant when the disturbance that they introduce is novel to the
ecosystem. One globally widespread example of this is the feral pig (Sus scrofa),
which is now present on all continents except Antarctica, and on many island
systems. When present, they cause significant physical disturbance through soil
turnover caused by foraging for roots and invertebrates. In forested ecosystems,
this activity can promote tree death, while in grasslands it can cause replacement of
perennial grasses with shorter-lived grasses and forbs, and greater incidence of
invasive plant species (Tierney and Cushman 2006). This disturbance regime has
also been shown to adversely affect major groups of microarthropods, whose dens-
ities recover only after pigs are removed from the system (Vtorov 1993). One of the
most impressive examples of the ecosystem effects of an invasive hervivore involves
the beaver (Castor canadensis) that has been deliberately introduced to Nothofagus-
dominated forest ecosystems in southern South America (Anderson et al. 2006, 2009)
(Fig. 5.16). Tree-felling and dam formation by these beavers has been described as
having the largest landscape-level impact on these ecosystems since the last ice age
(Anderson et al. 2009). Here, beavers eliminate riparian forest and reduce forest
canopy up to 30 m from stream edges (Anderson et al. 2006). This is accompanied by
the formation of meadows with higher herbaceous species richness, but with a much
greater incidence of exotic species. The belowground impacts of this transformation,
while unexplored, are likely to be substantial.
Some of the strongest ecosystem effects of invasive aboveground consumers
involve predators. Entry of a novel predator into an ecosystem often involves not
just the invasion event, but also the reduction or loss of its prey, sometimes to the
point of extinction. Invasive predators are present in most parts of the world, and
their impacts are most acute when they result in the removal of a consumer organism
that has an important role in the ecosystem itself. One such example involves
 = microbivores = microbi-detritivores = predators
Value of Index V
–1.0 –0.5 0 +0.5 +1.0
AUTOTROPHS P value
Browse layer <0.001
Ground layer 0.087
RESOURCE BASE
pH 0.193
C to N ratio 0.043
MICROFLORA
Microbial biomass 0.237
MICROFAUNA
Nematoda (microbe-feeding) 0.626
Rotifera 0.046
Copepeda 0.200
Nematoda (predaceous) 0.124
Tardigrada 0.111
MESOFAUNA
Enchytraeidae 0.372
Collembola 0.003
Oribatida 0.002
Astigmata <0.001
Mesostigmata 0.001
Prostigmata 0.020
MACROFAUNA
Corculionidae 0.050
Ptillidae 0.008
Hydrophylidae 0.028
Staphylinidae (litter feeding) 0.002
Gastropoda <0.001
Isopoda 0.003
Amphipoda <0.001
Diplopoda <0.001
Staphylinidae (predaceous) <0.001
Araenida <0.001
Pseudoscopionidea 0.043
Opiliones <0.004
Chilopoda <0.001

Fig. 5.15 Box-and-whisker plots summarizing data for the response to browsing mammals of
resources, autotrophs, and components of the decomposer food web in the litter layer, as assessed
by measurements performed inside and outside fenced exclosure plots for each of 30 locations
throughout New Zealand (see Wardle et al. 2001). The index V (Wardle et al. 2001), determined for
each response variable at each location, becomes increasingly negative if the value is increasingly
greater outside the exclosure relative to inside it, and increasingly positive if it becomes increasingly
greater inside the exclosure than outside it; the index ranges from 1 to þ1, with 0 indicating no
difference. For each variable, the box encompasses the middle half of the data (values of V)
between the first and third quartiles (i.e. 15 of the 30 locations); the bisecting line is at the value of
the median, and the horizontal line outside the box represents the typical range of data values.
Asterisks indicate outlier values. P values are for paired t-tests comparing the significance of
difference of the value of the variable inside compared with outside the exclosure across the 30
locations. From Wardle et al. (2001), with permission from the Ecological Society of America.
 (a)

(b)

Fig. 5.16 Substantial ecosystem transformation resulting from tree felling in Nothofagus forests
by invasive North American beavers (Castor canadensis) on Navarino Island in southern South
America. This disturbance is recognized by Anderson et al. (2009) as having the largest impact in
these forests since the last ice age. The images show (a) widespread death of high-elevation
riparian Nothofagus antarctica forest caused by beavers with no apparent regeneration and (b) a
low-elevation stream impounded by beavers, causing sedimentation and inundation of riparian
Nothofagus pumilio and Nothofagus betuloides forest. Images by C. Anderson.
 5.3 Species gains through invasion • 199

forested ecosystems on Christmas Island in the Indian Ocean. Here, the red land crab
(Geracoidea natalis) serves as the main consumer of seeds and seedlings, and as an
important processor of leaf litter (O’Dowd et al. 2003; Green et al. 2008). This
island has been invaded by the yellow crazy ant (Anoplolepis gracilipes) which
serves as a major predator of the crabs, thus eliminating the ecological role that the
crabs perform. The net result is enhanced tree seedling recruitment and reduced leaf
litter decomposition (O’Dowd et al. 2003). Another example involves the introduc-
tion of predatory foxes to the Aleutian Island chain, where they have caused
substantial reductions in nesting seabird colonies, thereby thwarting nutrient trans-
fer by the birds from the ocean to the land. Comparisons of islands that have been
invaded by foxes with those that have not have shown that predation of seabirds
causes a switch in the dominant vegetation from graminoids to low-lying forbs
and dwarf shrubs, reduced levels of soil and foliar nutrients, and altered flows
of nitrogen through aboveground consumer trophic levels (Croll et al. 2005;
Maron et al. 2006).
Invasive aboveground predators can also exert cascading effects on the below-
ground food web. This is apparent through studies on forested oceanic islands off the
coast of northern New Zealand. When seabirds occur on these islands in high
densities, they transfer nutrients from the ocean to the land, and cultivate soil with
their extensive burrowing activity during nesting periods. Several of these islands
have been invaded by alien rat (Rattus) species while several others have not, and
when present, the rats feed on seabird chicks and eggs, thereby severely reducing
seabird densities. As a consequence, invasion by rats reduces nutrient inputs by
seabirds to the soil, thereby adversely affecting many components of the soil food
web (Fukami et al. 2006; Towns et al. 2009) (Fig. 5.17) and processes driven by the
soil biota such as litter decomposition (Fukami et al. 2006). Further, reduced nutrient
inputs and densities of decomposer organisms on rat-invaded islands causes a
reduction in plant growth rates (Fukami et al. 2006), plant foliar and litter nutrient
concentrations, and rates of nutrient release from decomposing litter (Wardle et al.
2009b). Trees on rat-invaded islands also show greater resorption of nutrients by
plant leaves prior to litter fall (Wardle et al. 2009b), which is indicative of greater
nutrient limitation of the plants resulting from rat invasion. However, rats also reduce
soil disturbances and tree root damage caused by seabird burrowing activities, and for
this reason invasion by rats also results in a greater density of establishing tree
seedlings (Fukami et al. 2006; Mulder et al. 2009) and a higher tree standing biomass
(Wardle et al. 2007).
Before we leave the topic of invasive organisms, it is important to note that there
are many conspicuous examples of invasive organisms transforming both the above-
ground and belowground components of the ecosystem. These effects are inevitably
greatest when the invader has a particular capability that is lacking in the native biota,
and there are many examples of this across all major trophic groupings. Invasive
producers have particularly strong effects when they have an ability to fix nitrogen
that is lacking in the native biota, or when they can enter novel associations with soil
biota. Some invasive animals have important ecosystem effects through altering the
 200 • 5 Consequences of species losses and gains
Nutrients Producers Primary consumers Secondary consumers Tertiary consumers

10 (a) (d)
Herbivorous 6 Enchytraeids

Number g–1
Number g–1
nematodes
4
5
2

0 0
(e) Microbe-feeding 8 Predatory
15 (h)

Number g–1

Number g–1
SIR (mgCO2–C g–1 h–1)
nematodes nematodes
Higher 1.0 10
Soil (b) Microflora 4
fertilization plants ns
5
by ns
seabirds 0.5
0 0
20 (f) Rat– Rat–

Number g–1
Rotifers
free invaded
0
10 Island status

0
Log (number m–2)

Log (number m–2)

4 (c) 4
Minute land (g) Collembolans
Algae 3 snails 3
2 2
1 1
0 0
Rat– Rat– Rat– Rat–
free invaded free invaded
Island status Island status

Fig. 5.17 The response of components of the soil food web to invasion of rats (Rattus spp.) to oceanic islands in northern New Zealand. Here, the
rats eat the chicks and eggs of the seabirds and therefore thwart the transfer by seabirds from the ocean to the land. Data are means + SE for nine rat-
free (seabird-dominated) islands and nine rat-invaded islands, *, **, and *** mean P < 0.05. 0.01, and 0.001 respectively; SIR, substrate-induced
respiration, used as a relative measure of microbial biomass. From Fukami et al. (2006), with permission from Wiley-Blackwell.
 5.4 Consequences of global change • 201

physical structure of ecosystems (e.g. invasive earthworms, beavers, and pigs), or

through consuming native plant and animal species that themselves perform import-
ant functions in the ecosystem. Although most alien organisms entering a new
ecosystem probably perform a relatively minor role (Thompson et al. 1995), there
are now many examples, including those described above, that provide convincing
evidence that a subset of the alien biota is nevertheless able to radically transform
ecosystems, often to an alternative stable state.

5.4 Consequences of global change through

causing species gains and losses
In the preceding sections of this chapter, we have considered the consequences of
species losses and species gains (principally through invasions), for aboveground and
belowground biota and the ecosystem processes that they drive. As we have dis-
cussed, the most important causes of species loss and gain are habitat destruction and
land-use change, and biological invasion. However, there is also mounting evidence
that other global change phenomena, including climate change, can act as important
drivers of species loss with potentially far reaching consequences for aboveground
and belowground properties of ecosystems, and climate feedbacks. For example,
climate envelope models (which are based on species environmental preferences)
predict severe loss of biodiversity due to climate warming (Thomas et al. 2004;
Thuiller et al. 2005), largely because species are unable to disperse during the
timescale of climate change. Moreover, climate change can cause species loss by
affecting species phenology and interaction strengths, which can lead to mismatches
in the life histories of consumers and their resources (Post and Forchhammer 2008)
and decoupling of trophic interactions on which they rely (e.g. Fox et al. 1999; Visser
and Both 2005; Memmott et al. 2007). As discussed earlier in this chapter, such losses
of species and resulting changes in community composition could have important
implications for the belowground subsystem and ecosystem processes, especially
when the physiological traits of those species that are lost differ markedly from those
that remain.
Another important route by which climate change can indirectly influence ecosys-
tems processes is through causing range expansion of species into new territories.
Although species range shifts can be caused by changes in land use, the well-
documented expansion of many species towards higher latitudes and altitudes over
the past few decades strongly suggests that climate warming plays a significant role
(Walther et al. 2002; Parmesan and Yohe 2003). For example, climate warming has
been proposed as the cause of widespread upward movement of alpine plant species
(Klanderud and Birks 2003; Walther et al. 2005; Lenoir et al. 2008; but see Wilson
and Nilsson 2009) and advance in the alpine treeline (Kullman 2002; Kullman and
Öberg 2009), although a recent global meta-analysis indicates that treelines are
not universally responding to climate warming (Harsch et al. 2009). As discussed
in Chapter 3, climate warming has also been proposed as the cause of the northward
202 • 5 Consequences of species losses and gains

expansion of boreal forest into Canadian tundra (Danby and Hik 2007) and
pan-Arctic shrub encroachment in Arctic tundra (Sturm et al. 2001; Epstein et al.
2004; Tape et al. 2006; Wookey et al. 2009). Also, the northward and upward
migration of many vertebrate and invertebrate species in Britain (Hickling et al.
2006; Menendez et al. 2007) (Fig. 5.18), and small mammals (Moritz et al. 2008)
and invertebrates, such as the mountain pine beetle (Logan and Powell 2001;
Williams and Liebhold 2002), in North America has been attributed to climate
warming. As will be discussed below, some of these range shifts and consequent
changes in the diversity and composition of communities have the potential to
strongly modify ecosystem process of the territories that they invade, with, in some
cases, far-reaching consequences for carbon-cycle feedbacks.
Many biotic factors determine the ability of different species to shift their ranges
under climate warming, such as dispersal ability, habitat specificity (Warren et al.
2001; Menendez et al. 2006, 2007) and availability (Hill et al. 2001), and escape from
natural enemies (Menendez et al. 2008). Most work on this has been done from an
aboveground perspective, but there is now emerging evidence that belowground biota

100
Average northward shift of the range margin (km)

Recorded
90 Well-recorded
80 Heavily recorded

70

60

50
40

30

20

10

0
en

gs

es

s
al

rd

lie

lie

le

le

er

lie
ic
ed
in
tm

et

et

dl
m

id
Bi

al

rf

al
ew

ip
be

be

oo
am

Sp
tte
es

d
ill
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v

an

an
W
Bu

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d
M

La

M
ar

un
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H

rs

s
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ro
pe

ng

et
G
op

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Lo
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ld
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So

Taxonomic group

Fig. 5.18 Latitudinal shifts since the 1960s in the northern range margins of 12 taxonomic
groups of terrestrial environments in Great Britain, at a 10-km-grid-square resolution. The
groups analysed were grasshoppers and allies (Orthoptera), lacewings (Neuroptera), butterflies
(Rhopalocera), spiders (Araneae), mammals (Mammalia), woodlice (Isopoda), ground beetles
(Carabidae), harvestmen (Opiliones), millipedes (Diplopoda), longhorn beetles (Cerambyci-
dae), soldier beetles and allies (Cantharoidea and Buprestoidea), and birds (Aves). Results are
given for three levels of sub-sampling of data, namely recorded, well-recorded, and heavily
recorded (see key). From Hickling et al. (2006), with permission from Wiley-Blackwell.
 5.4 Consequences of global change • 203

might also play a role in affecting range expansion of species under change. For
example, it was recently shown by Engelkes et al. (2008) that range-expanding plant
species are better defended against shoot and root enemies than are related native
plant species growing in the same habitat, suggesting that successful range expanders
may experience less control by aboveground or belowground enemies than the
natives. Another mechanism that might influence the ability of certain species to
expand into new territories under climate change concerns species-specific coupling
of plants with soil biotic communities. As discussed in Chapter 3, there is often a high
degree of specificity between individual plants species and the soil biotic community;
for example, there is some evidence that certain plant species can preferentially select
for decomposer taxa that enhance the decomposition of their own litter (e.g. Hansen
1999; Vivanco and Austin 2008; Ayres et al. 2009), indicative of feedback mechan-
isms. As a consequence, it is possible that the expansion of such species under
climate change will disrupt such specialism in aboveground–belowground inter-
actions, with possible consequences for their growth and competitive interactions
in new territories. This idea has, however, only started to be tested very recently (e.g.
Van Grunsven et al. 2007, 2010; Engelkes et al. 2008).
Relatively little is known about the consequences of range-expanding species for
soil biota and ecosystem processes. As discussed in Chapter 3, the main route by
which climate-driven shifts in plant species influence soil organisms is likely to be
via changes in the quality and quantity of organic matter entering the soil, and
through modifying the soil physical environment, for example by changes in root
architecture and rooting depth (Jackson et al. 1996). One of the best documented
examples of the consequences of climate-driven range expansion for ecosystem
processes and carbon-cycle feedbacks is the expansion of dwarf-shrubs northward
in the Arctic upwards in alpine regions (see Wookey et al. 2009). As discussed in
Chapter 3, dwarf-shrubs produce woody litter of much poorer quality, and hence
lower decomposability, than the graminoids and forbs that they replace (Cornelissen
1996; Quested et al. 2003; Dorrepaal et al. 2005). This may in turn slow down rates
of decomposition and, potentially, counteract the direct enhancement of decompos-
ition by warming and consequent loss of carbon from Arctic soils (Cornelissen et al.
2007). However, as highlighted in the discussion of this topic in Chapter 3, shrub
expansion in the Arctic will also affect several other factors that influence rates of
carbon cycling in Arctic soils, such as rooting depth, the incidence of fire, and snow
cover. Moreover, as recently shown by Olofsson et al. (2009), shrub expansion in a
warmer Arctic might be limited by biotic factors such as reindeer grazing. Therefore,
as emphasized in Chapter 3, the role of biotic factors and interactions should be
considered in order to understand how a changing climate will influence shrub
expansion and carbon-cycle feedbacks in tundra ecosystems (Olofsson et al. 2009;
Wookey et al. 2009).
Another case of shrub expansion concerns that which is occurring in arid and semi-
arid grassland ecosystems throughout the world (Schlesinger et al. 1990; Peters et al.
2006; Throop and Archer 2008; Maestre et al. 2009). Shrub expansion in these
ecosystems has been attributed to a variety of factors, including overgrazing, the
204 • 5 Consequences of species losses and gains

suppression of fire and climate change (Archer et al. 1995; Van Auken 2000), and can
lead to increased heterogeneity in soil resources due to the formation of ‘islands’ of
fertility beneath shrub patches and impoverished inter-canopy areas (Schlesinger and
Pilmanis 1998). In some situations, such as in the Chihuahuan Desert, USA, this
process has been shown to create a feedback that ultimately leads to the desertifica-
tion of the ecosystem (Schlesinger et al. 1990), a process that can be further
exacerbated by factors such as climate change and over-grazing (Verstraete et al.
2009). However, this process does not appear to be universal. For instance, in the
Mediterranean region, recent shrub encroachment into Stipa tenacissima dominated
grasslands has been shown to be an important step in the reversal of desertification
processes (Maestre et al. 2009). This encroachment, albeit caused by land abandon-
ment rather than climate change, was found to enhance amounts of carbon and
nitrogen in soil, and rates of nitrogen mineralization in soil beneath both shrub and
Stipa canopies, and also in bare ground areas.
In general, there is much uncertainty about how shrub encroachment affects the
belowground subsystem and soil carbon and nutrient pools, with both negative
(Schlesinger et al. 1990; Jackson et al. 2002) and positive (Throop and Archer
2008; Maestre et al. 2009) responses being detected. Moreover, differences in
shrub impacts on ecosystem carbon storage appear to vary under different climatic
conditions. For example, in a study of eight North American graminoid-dominated
ecosystems invaded by shrubs that covered a four-fold range in mean annual pre-
cipitation, from Arctic tundra to Atlantic coastal dunes, Knapp et al. (2008) found that
shrub invasion decreased aboveground NPP, and hence carbon input, in drier sites,
but dramatically increased aboveground NPP in regions with high mean annual
precipitation (Fig. 5.19). In contrast, however, Jackson et al. (2002) studied woody-
plant invasion along a precipitation gradient in south-western USA, and found a
strong negative relationship between precipitation and changes in soil organic carbon
content: woody-plant invasion into drier sites resulted in soil carbon gain, whereas in
wetter sites it caused soil carbon loss. As suggested recently by Maestre et al. (2009),
such variation in the impact of shrub encroachment on carbon dynamics is likely due
to differences in the traits of the woody vegetation in different climatic regions, which
as discussed in Chapter 3 act as a key determinant of plant effects on the belowground
subsystem. It is widely acknowledged that much remains unknown about the influ-
ence of shrub encroachment on the belowground subsystem and carbon-cycle feed-
backs (Jackson et al. 2002; Knapp et al. 2008; Maestre et al. 2009), and further work
is needed on this issue, especially given the global extent of shrub encroachment and
the potential for climate change to exacerbate this phenomenon.
Recent evidence also points to significant effects of range expansion of herbivores
on ecosystem carbon dynamics. With regard to herbivorous insects, Kurz et al.
(2008) used simulation models to estimate that the recent outbreak of the mountain
pine beetle (Dendroctonus ponderosae) in British Columbia, Canada, which is an
order of magnitude larger in area and severity than all previous outbreaks (Taylor
et al. 2006; Williams and Liebhold 2002), converted the forest from a small net
carbon sink to a large net carbon source, both during and immediately after the
 5.4 Consequences of global change • 205

(a)

1000
1200

Mean ANPP (g m–2)

800 Grassland
Shrubland
1000 600 P < 0.05

400
800
ANPP (g m–2)

200

0
600
Grassland
Change
400
shrublands
200

0
Mean annual precipitation

CHI SBS TUN SAV THW TGP ISL

Sites
(b)

1200 ISL
Change in ANPP (g m–2)

1000 TGP
THW

800
r 2 = 0.80
600

400 TUN

200
SAV
0 CHI
SBS
200 400 600 800 1000 1200
Precipitation (mm)

Fig. 5.19 Response of aboveground NPP (ANPP) to shrub encroachment in North American
grasslands. (a) Patterns of ANPP in grasslands (black bars) and former grassland sites now
dominated by shrubs (open bars) along a gradient of mean annual precipitation, showing that
the largest responses in ANPP to shrub conversion occur in the most mesic sites (the inset
shows the mean increase in ANPP over all sites with shrub encroachment into grasslands).
(b) The relationship between mean annual precipitation and the change in ANPP for seven sites
across North America where grassland has been converted to shrubland. Solid line indicates a
significant positive relationship between mean annual precipitation and the change in ANPP.
Sites codes, along the gradient of increasing mean annual precipitation, are: Chihuahuan Desert
(CHI); sagebush steppe (SBS); tussock tundra (TUN); subtropical savanna (SAV); subtropical
thorn woodland (THW); tallgrass prairie (TGP); and Barrier Island (ISL). From Knapp et al.
(2008), with permission from Wiley-Blackwell.
206 • 5 Consequences of species losses and gains

outbreak (Fig. 5.20). This was attributed to a reduction in photosynthetic capacity

(and hence carbon uptake) caused by widespread tree mortality, combined with an
increase in heterotrophic respiration derived from the decomposition of dead trees.
Importantly, the impacts of the outbreak on carbon emissions over 21 years was
calculated to exceed that due to other factors, such as forest fire, and to be
comparable to 5 years of greenhouse gas emissions from Canada’s transportation
sector (i.e. 200 Mt carbon dioxide equivalents in 2005). Although the increased
extent and severity of the outbreak has been attributed in part to an increased area in

(b) (a)

(c)

0 75 150 300 km

Fig. 5.20 Geographic extent of mountain pine beetle (Dendroctonus ponderosae) outbreak in
North America. (a) Extent (dark grey) of mountain pine beetle. (b) The study area includes 98%
of the current outbreak area. (c) An area of pine forest subject to tree mortality caused by pine
beetle outbreak. Although not visible in the image, pine trees turn red in the first year after
beetle kill and grey in subsequent years. From Kurz et al. (2008), with permission from
Macmillan Publishers Ltd. Ó 2008 Her Majesty the Queen in right of Canada, Natural
Resources Canada, Canadian Forest Service as originally published in Nature.
 5.4 Consequences of global change • 207

the host tree (i.e. mature pine stands), it is also widely attributed to climate change,
which has led to an expansion of the outbreak northward and into higher elevation
forests (Taylor et al. 2006; Williams and Liebhold 2002). As noted by Kurz et al.
(2008), evidence of climate change related increases in the extent or severity of
forest insect disturbance is mounting, and future climate change could facilitate
further range expansion; failure to account for their impacts could therefore result in
overestimation of the potential for forests to offset anthropogenic carbon dioxide
emissions.
Range expansion and subsequent overabundance of mammalian herbivores has
also frequently been observed, particularly for various species of deer in forest,
grassland and tundra (Côte et al. 2004). For example, sika deer (Cervus nippon)
have expanded their range through Japan by nearly 70% over the past two decades
(Takatsuki 2009). The relative importance of different agents of global change in
influencing range expansion of deer is poorly understood, but climate change is
predicted to contribute to both range expansion and contraction of the major herds
of caribou (Rangifer tarandus) on the Québec-Labrador peninsula through affecting
snowfall patterns, food (notably lichen) availability, local-scale temperature, fire
regime, and abundance of blood-sucking insects (Sharma et al. 2009). Enhanced
range expansion of deer species in both forest and tundra may lead to large shifts in
vegetation composition (Côte et al. 2004; Takatsuki 2009), which as described in
Chapter 3 can have important knock-on effects on ecosystem processes, including
those relevant to carbon sequestration. While the impacts of deer on ecosystem
processes in newly colonized areas following range expansion and subsequent
population growth has been little studied, we would expect these effects to have
fundamental similarities to those frequently observed as a consequence of deer
invasion and overabundance (Wardle and Bardgett 2004), as described earlier in
this chapter.
Much is still to be learned about the different ecological traits and mechanisms
responsible for range shifts, which are taking place in the context of not just climate
warming, but also land use and other environmental changes (Hickling et al. 2006).
Moreover, little is known about the consequences of range shifts for community and
ecosystem properties, although, as discussed above, evidence is mounting that
species-range shifts are widespread across taxonomic groups and geographic regions.
It is also increasingly recognized that, in some cases, these shifts can have significant
consequences for both the composition and functioning of the aboveground and
belowground subsystems, and ultimately climate carbon-cycle feedbacks. However,
as also highlighted above, the scale of such impacts will vary greatly depending on a
variety of factors, such as the traits of those species that are shifting in their range and
the environmental conditions and heterogeneity of the habitats into which they
invade, which may also be affected by climate change, as discussed in Chapters 2
and 3. Therefore, a major challenge for the future will be to understand the mechan-
isms by which climate change simultaneously impacts on terrestrial ecosystems
through range shifts and through its direct and indirect effects on resident above-
ground and belowground communities.
208 • 5 Consequences of species losses and gains

5.5 Conclusions
In Chapters 2–4 we emphasized how the functioning of terrestrial ecosystems is
driven by the community composition of plants, the soil biota, herbivores, and their
predators, as well as the interactions among these organisms. However, as empha-
sized throughout this chapter, the species composition of communities does not
remain constant over time, and species can be both gained and lost. While these
losses and gains do occur naturally, the rates of both processes are being enhanced by
several orders of magnitude through human activities. Consequently, communities
can be simultaneously losing some species and gaining others, leading to substantial
shifts in both structural and functional attributes of the community. In this chapter, we
have provided multiple examples across a range of taxa and ecosystems to highlight
both how species losses and gains can impact upon aboveground and belowground
biota and their linkages, as well as the consequences of this for the functioning of the
ecosystem.
Most studies that have aimed to understand how species losses in real ecosystems
affect processes have utilized experiments in which species richness is experimen-
tally varied as a treatment, with species at each richness level often chosen at random
from a species pool. Despite the enormous research effort devoted to this approach
over the past decade, our understanding of the effects of biodiversity loss that occurs
in real ecosystems through human-induced changes in both biotic and abiotic factors
remains poor. Moreover, as we highlight in this chapter, evidence for strong and
consistent causative effects of species diversity on ecosystem processes remains
limited, especially when the belowground subsystem is considered. Instead, there is
growing evidence for diversity effects being ‘context-dependent’ in that biodiversity
effects on ecosystem processes vary greatly according to environmental context (e.g.
Fridley 2002; Hättenschwiler and Gasser 2005; Jonsson and Wardle 2008). Further,
there is increasing recent recognition that species richness manipulation experiments
may not realistically represent how ecosystem processes are affected by loss of
species in real ecosystems, because species are not lost from real communities
randomly (Wardle 1999; Leps 2004; Ridder 2008). In this chapter, we therefore
argue that an improved understanding of the aboveground and belowground conse-
quences of biodiversity loss requires experiments to be done in real ecosystems, and
that this is best achieved through ‘removal experiments’ in which species are
experimentally removed from real ecosystems so as to represent real loss of species
or functional groups resulting from changes in abiotic and biotic extrinsic factors
caused by human activity (Díaz et al. 2003; Wardle and Zackrisson 2005; Suding
et al. 2008; Ward et al. 2009). We have highlighted the utility of this approach by
presenting examples of how experimental removals of taxa of plants, soil microbes
and fauna, and aboveground consumers can affect key ecosystem processes both
above and belowground. Such studies, together with investigations of ecosystem
effects of actual species losses (e.g. Zimov et al. 1995; Ripple and Betscha 2006),
highlight that ecosystem processes are likely to be influenced primarily by differences
in key characteristics or traits between species that are lost and those that remain.
 5.5 Conclusions • 209

There has been much recent work, and some significant advances, in understand-
ing how gains of species through invasion in real ecosystems affect aboveground–-
belowground linkages and ecosystem processes. In particular, several studies
comparing coexisting native and invasive species or floras have demonstrated im-
portant differences between them in terms of functionally important traits (Baruch
and Goldstein 1999; Leishman et al. 2007), effects on decomposition and mineral-
ization processes (Ehrenfeld 2003), and feedback interactions involving the soil biota
(Klironomos 2002). Recent studies have also highlighted that invasive plants may
undergo different interactions with both soil biota and other plant species in their new
habitat than in their native range (Reinhart et al. 2003; Wolfe and Klironomos 2005),
which in turn can contribute to the invader’s success. While the majority of studies on
invader effects on aboveground–belowground linkages have focused on invasive
plants, in this chapter we highlight several recent examples that reveal the capacity of
invasive consumers to transform ecosystems when they have key functional capabil-
ities that are lacking in the native biota. Some of the most spectacular examples we
describe involve invasive herbivores such as beavers, deer and gypsy moths, invasive
predators such as ship rats, foxes, and ants, and invasive soil animals such as earth-
worms and flatworms. Further, we highlight that global climate change is not only an
important driver of species gains and losses in ecosystems through inducing shifts in
phenlogy and interaction strengths, but also by causing range expansion of many taxa
towards higher latitudes and elevations. Although comparatively few examples have
considered range-expanding species from an aboveground–belowground perspective,
recent studies have shown that that such species can have important effects on
ecosystem properties and potentially carbon-cycle feedbacks (e.g. Knapp et al. 2008;
Kurz et al. 2008), and may show different interactions with their antagonists to related
native species in the new or expanded range (Engelkes et al. 2008).
Despite much recent effort on understanding how species gains and losses affect
ecosystems, our knowledge of how species loss affects ecosystem processes remains
limited, largely because relatively few studies have considered the impacts of non-
random species losses in real ecosystems and how they vary in different environment
contexts. We argue that the most productive way forward would be the widespread use
of experimental or theoretical approaches that directly investigate how loss of species
with functionally important traits directly impact upon other organisms and ecosystem
processes, and whether traits that predispose species to become extinct from a
community are also those that drive ecosystem processes. With regard to invasive
biota, although we have a reasonable understanding of how ingress of new plant
species affects aboveground and belowground processes, much remains unknown
about the mechanisms involved, and how these mechanisms may contribute to the
spread of the invader. While interesting mechanistic theories (e.g. the novel weapons
and enemy escape hypotheses) have been suggested, our understanding of their
ecological significance remains limited. The issue of how invasive plants exert
ecological effects through not just their per-capita effects but also the rate and extent
to which they increase their range and abundance remains little explored, even though
such information is crucial to predicting the ecosystem-level consequences of
210 • 5 Consequences of species losses and gains

biological invasions over time. Further, while a growing number of studies have
recognized the impacts of animal invasions both aboveground and belowground, we
have yet to move away from accumulating a collection of intriguing examples to
developing strong predictive or conceptual frameworks for understanding how inva-
sive animals affect ecosystems. Finally, we are only beginning to understand the
ecological consequences of range-expanding species in new habitats resulting from
global change (e.g. global warming), and an important challenge will be to understand
how range expansion and its ecological consequences are driven by species traits and
interactions, as well as the biotic and abiotic characteristics of the environment.
6
Underlying themes and ways forward

6.1 Introduction
Our aim in this book was to draw attention to the importance of biotic interactions
between aboveground and belowground communities as fundamental drivers of
community dynamics and ecosystem functioning. Although having a long history,
this area of research has seen tremendous amount of activity over the past two
decades and has yielded several recent conceptual advances, as apparent in the
preceding chapters. These developments have arisen through increasing recognition
that the aboveground and belowground subsystems do not work in isolation, but
rather that they are strongly interdependent. Feedbacks between the aboveground
and belowground subsystems emerge through plants interacting both with decom-
posers via the indirect pathway and with root-associated organisms (e.g. pathogens,
root feeders, and mycorrhizal fungi) via the direct pathway, with these interactions in
turn being influenced by fauna that feed on plants, microbes, and on each other
(Fig. 2.1). While it is certainly true that historically there have been ecologists who
have fully acknowledged that understanding aboveground processes requires explicit
recognition of those that occur belowground, and vice versa (e.g. Müller 1884;
Handley 1954; Vitousek and Walker 1989), over the past few years recognition of
this issue has been the norm rather than the exception. This recognition has facili-
tated a great deal of recent research that has contributed to better understanding of the
feedbacks and interactions that take place in the plant–soil system and the ecosystem
processes that they drive; this book provides an up-to-date synthesis of this under-
standing.
We have addressed the issue of aboveground–belowground feedbacks by high-
lighting four key components: biotic interactions in the soil (Chapter 2); plant
community influences (Chapter 3); the role of aboveground consumers (Chapter 4);
and the influence of species gains and losses (Chapter 5). While these topics remain
as discrete entities around which the book is structured, there are a number of
cross-cutting themes that run throughout those chapters; in this chapter we focus on
these themes. These themes fall into three distinct but complementary categories
that operate at different spatial and temporal scales. The first involves biotic
interactions and feedbacks that occur at local scales (i.e. the scale of the individual
organism) and their consequences for ecosystem processes. The second occurs at
larger spatial and temporal scales, and involves characterizing variation both
aboveground and belowground over space and time, as well as what drives
212 • 6 Underlying themes and ways forward

differences among contrasting ecosystems. The third involves considering linkages

between the aboveground and belowground subsystems in relation to human-
induced global change phenomena, such as climate change. Through considering
these cross-cutting themes in this chapter, we aim to explicitly highlight areas of
significant recent development, as well as those that we believe are productive
avenues for future research.

6.2 Biotic interactions, feedbacks, and

ecosystem processes
6.2.1 Linkages and feedbacks between the aboveground and
belowground subsystems
It has long been known that the type of plant species present affects the soil
community, and that components of the soil community in turn affect the plant
community. As such, feedbacks between the plant and soil communities are inevit-
able. A core element of this book has been to highlight the positive and negative
effects that plant and soil communities can have on each other, and therefore to
develop insights about feedbacks between these communities. As emphasized
throughout the book, and as depicted in Fig. 2.1, soil communities consist of a myriad
of organisms that interact with plants both via the indirect pathway (i.e. decomposers)
and the direct pathway (including root-associated pathogens, root herbivores, and
mycorrhizal fungi). A large and growing number of recent studies have used standard
feedback-experiment methodology (Chapter 3) to investigate the net strength
and direction of feedbacks between plants and their associated soil biota. As highlighted
in Chapters 2, 3, and 5, such experiments have greatly advanced our understanding of
how these feedbacks may influence plant species replacement (Packer and Clay 2000)
and succession (Kardol et al. 2006), success of invasive plants (Klironomos 2002;
Reinhart et al. 2003), and plant range expansion under global change (Engelkes et al.
2008). Such studies emphasize that the strength and direction of feedbacks between
plants and their soil biota may differ greatly among plant species with different attributes,
and highlight that the soil community is a major driver of plant species dynamics and
the balance of interactions between coexisting plant species.
Although many plant–soil feedback studies point to negative feedbacks (Kulmatiski
et al. 2008), we suggest in Chapter 3 that current methodology is more likely to
encourage soil biota that undergo negative rather than positive associations with the
soil biota. Further, the majority of feedback studies have focused on early succes-
sional and herbaceous plant species which are more likely to show negative associ-
ations with soil organisms than are late successional and woody species. As we
discuss in Chapters 2 and 3, mycorrhizal fungi frequently enter into positive associ-
ations with components of the plant community, and this may be especially true for
forests dominated by one or a few species of ectomycorrhizal tree species. Further, if
plant species do indeed promote decomposer communities that preferentially miner-
alize their own plant litter as opposed to that of other plant species (including those
 6.2 Interactions, feedbacks, and processes • 213

with which they coexist; e.g. Vivanco and Austin 2008), then this makes positive
feedbacks between plant species and their decomposer biota likely and probably
widespread. Determining the net magnitude of feedback of the diverse components of
the soil community (including those not favoured in current soil-feedback method-
ologies) with their associated plant species, and understanding how this contributes to
plant community dynamics and ultimately ecosystem processes, remains one of the
main unresolved challenges in this field.
Both plants and those soil organisms with which they directly interact are consumed
by fauna, and trophic relationships that involve fauna are important drivers of above-
ground–belowground associations. As such, several studies have shown the indirect
effects of soil fauna and faunal community structure on plants and their aboveground
consumers (Chapter 2), and of foliar herbivores on belowground processes (Chapter 4).
A growing number of studies have also characterized belowground responses to losses
of herbivore species, invasive herbivores, and herbivore range expansion (Chapter 5).
Recent advances have involved not only quantifying the aboveground or belowground
effects of herbivorous fauna, but also the mechanistic basis through which their effects
occur (e.g. Mikola et al. 2009; Sørensen et al. 2009) and feedback to plant growth
(Hamilton and Frank 2001; Hamilton et al. 2008). However, studies of this type are still
at their infancy, and further research is needed to determine the relative importance of
different herbivore-driven mechanisms and feedbacks across contrasting ecosystems.
Further, there is growing recognition that upper-level consumers (i.e. predators of
herbivorous and microbe-feeding fauna), both aboveground and belowground, have
the potential to induce trophic cascades that can indirectly influence organisms on the
other side of the aboveground–belowground interface, sometimes considerably. In this
light, recent studies have provided spectacular examples of how invasions of islands by
aboveground predators, such as ship rats (Fukami et al. 2006), foxes (Maron et al.
2006), and ants (O’Dowd et al. 2003), have exerted cascading effects that profoundly
affect the plant community, soil fertility, and feedbacks to plant growth (Chapter 5).
However, studies on how top predators (including predator invasion and extinction)
affect ecosystem functioning are still relatively few (see Chapters 2, 4, and 5), and
much remains unknown about the extent to which recent examples in the literature
represent special cases as opposed to widespread phenomena. As such, there is still a
significant need for a more fully developed multitrophic perspective about how
interactions on both sides of the aboveground–belowground interface affect the func-
tioning of terrestrial ecosystems.
Central to understanding aboveground–belowground interactions and feedbacks is
the need to know the extent to which plant community structure serves as a deter-
minant of soil community structure and vice versa. Over the past decade, several
studies have made some headway in determining the degree to which the structure of
the two communities is associated (Chapters 2 and 3), as well as the extent to which
their diversities are coupled (reviewed by Wardle 2006). However, one major
challenge that continues to impair progress on this topic involves difficulties in
adequately quantifying soil community structure, particularly at taxonomically fine
levels of resolution. There are obvious taxonomic problems in characterizing the
214 • 6 Underlying themes and ways forward

community structure of much of the soil biota. Indeed, over 90% of microfloral and
microfaunal species probably remain undescribed, and over the past few years there
has been an increasing dearth of taxonomists that are well qualified to identify
mesofaunal and smaller organisms. These impediments serve as a major reason as
to why many ecologists and soil scientists over the past decades have continued to
describe the soil community as a ‘black box’. One way forward is the recent
development of molecular approaches that have the potential to describe soil com-
munities in a manner that has not existed historically. Traditional PCR-based
molecular techniques for assessing microbial communities (e.g. denaturing-gradient
gel electrophoresis (DGGE), terminal restriction fragment length polymorphism
(TRFLP)) have provided lists of what soil organisms are present in soil, but generally
not their relative abundances, limiting their utility for addressing ecological questions
or their sensitivity for detecting microbial community responses to environmental
factors (Ramsey et al. 2006). However, new techniques based on 454 pyrosequencing
(Goldberg et al. 2006; Hudson 2008) offer much potential for determining how
microbial community composition may respond to biotic and abiotic factors at
much finer levels of resolution than has been the case to present. Such approaches
have recently been used to reveal an unexpectedly high diversity of microbes in
terrestrial ecosystems, for instance of fungi in soil (Buée et al. 2009) and in the
phyllosphere of temperate trees (Jumpponen and Jones 2009), and contrasting levels
of bacterial diversity between rhizosphere and bulk soil (Uroz et al. 2010). Such
approaches, and the vast quantity of data that they generate, provide ecologists with
opportunities to describe microbial communities in greater detail than has been the
case previously, and could greatly advance our understanding of how plant and soil
communities are linked.

6.2.2 Organism traits as ecological drivers

There is a long history in plant ecology of characterizing how plant traits differ
among species with different ecological strategies (Grime 1977, 1979). As discussed
in Chapter 3, it is now well recognized that among plant species there is a primary
axis of evolutionary specialization ranging from those with traits associated with
rapid resource capture, to those that have traits linked to resource conservation
(Grime et al. 1997; Díaz et al. 2004). Of particular relevance to this book is the
recognition that these traits (and trait differences among species) are important
drivers of ecosystem processes and properties. This is because they determine litter
and foliar quality, the decomposability of root, shoot, and stem litter (Chapter 3), the
palatability and consumption of foliage (Chapter 4), and, ultimately, nutrient cycling
and feedbacks between the aboveground and belowground subsystems (Chapters 3
and 4). As such, they serve as the agents through which differences between dominant
species influence how ecosystems function. Further, as discussed in Chapter 5,
invasive plant species can differ greatly in key functional traits from the native
species of the invaded community, with potentially important ecosystem-level con-
sequences. The same may also be true for plant species that are lost from a community,
 6.2 Interactions, feedbacks, and processes • 215

although as discussed in Chapter 5 this issue is less well understood. One important
recent advance in this topic is the recognition that there can be tremendous variation
in key functional traits even at very local scales (Hättenschwiler et al. 2008), which
can be almost as great as the magnitude of variation observed globally (Richardson
et al. 2008). As such, there is evidence that rates of litter decomposition are influenced
more by trait differences among species, even at very local scales, than by macrocli-
matic variation across biomes (Cornwell et al. 2008). Further, a number of recent
publications are now recognizing that plant species trait differences can be important
predictors of differences in ecosystem functioning across communities (e.g. Vile et al.
2006; Fortunel et al. 2009) and of how human activities may affect ecosystems and
the delivery of ecosystem services (e.g. Díaz et al. 2007; De Deyn et al. 2008).
Despite the considerable interest in the ecological significance of plant traits, there
are several important issues which remain little understood, and which are only now
beginning to gain attention. Here we highlight three issues raised in Chapter 3 that
deserve particular emphasis. First, most ecosystem-centred studies have focused on
foliar traits, and much remains unknown about how traits of other tissues that may
represent a large proportion of ecosystem NPP, such as roots, stem tissues, and
(in forested areas) wood, can drive ecological processes either aboveground or
belowground (but see Weedon et al. 2009; Cornwell et al. 2009). Second, most
studies have focused on traits of higher plants, yet in many ecosystems worldwide
mosses and ferns also serve as important drivers, and in many boreal forests and the
tundra mosses can represent a substantial proportion of total NPP. However, the
issue of how moss and fern traits might affect ecological processes has been
addressed only in a few studies, and mostly in relation to litter decomposition
(e.g. Wardle et al. 2002 and Amantangelo and Vitousek 2008 for forest ferns;
Dorrepaal et al. 2005 and Lang et al. 2009 for sub-Arctic mosses). Third, the vast
majority of studies on plant traits have been at either the species or functional-group
level of resolution. As discussed in Chapter 3, some plant species show considerable
intraspecific phenotypic or genotypic variation of both foliar and litter quality, but
little is known about whether functionally important traits vary within species in a
similar way to that often found across species. Large differences among genotypes
within species have been shown for both litter decomposability and foliage palat-
ability (e.g. Classen et al. 2007; Silfver et al. 2007), and it is therefore likely that
there is an ecologically meaningful level of variability of traits within some species,
especially those that occupy vastly contrasting environments. However, rigorous
testing of this idea remains minimal.
A major issue that remains poorly understood is how plant traits influence
consumer organisms, their community structure, and their ecosystem impacts both
belowground and aboveground. At a coarse level, it is recognized that bacterial-
based and fungal-based energy channels in soil food webs vary greatly in their
effects on nutrient cycling (Chapter 2), and that plant trait combinations can influ-
ence which of the two energy channels dominate (Chapter 3; Fig. 4.3). Further,
animal body size distribution can vary greatly among ecosystems (Mulder and Elser
2009) which should in turn influence soil processes (Chapter 2), although almost
216 • 6 Underlying themes and ways forward

nothing is known about how this is affected by traits of dominant plant species. At a
finer resolution, coexisting fungi differ greatly in traits that determine their metabolic
capacity, and for major faunal groups, such as Nematoda and Acari, functionally
important traits relating to feeding structures and mouthparts vary greatly among
species. While these traits are undoubtedly crucial in driving belowground inter-
actions and processes, very little is known about how plant effect traits select for soil
community structure, or determine the trait distribution of the soil community.
However, an enhanced knowledge of this is essential for advancing our understand-
ing of how aboveground–belowground linkages at the community level drives
ecosystem functioning. Although aboveground plant traits are increasingly being
recognized as important determinants of how plant communities interact with herbi-
vores (Díaz et al. 2006), as discussed in Chapter 4, the issue of how plant traits select
for herbivore communities and herbivore trait distributions remains essentially
unexplored. In sum, much remains to be determined as to how suites of plant traits
select for consumer traits (either aboveground or belowground) that may in turn be
important in driving ecosystem processes and have consequences for higher trophic
levels.
One issue for where a trait-based approach could usefully inform is in terms of
understanding ecosystem processes for multiple-species communities. As out-
lined in Chapter 3, weighted trait average approaches (in which trait values of
each species in a community are weighted in terms of their relative abundance)
have recently been used to predict both plant productivity (Vile et al. 2006) and
rates of decomposition (Quested et al. 2007; Fortunel et al. 2009) at the commu-
nity level. However, as we discuss in Chapter 3, such approaches have limitations
for understanding the effects of non-additive interactions among component
species on ecosystem processes. To date, this issue has attracted limited attention,
although some studies have focused on quantifying how ecosystem-level pro-
cesses can be influenced by the magnitude of trait variation among coexisting
species of live plants (Hooper et al. 2005), decomposer invertebrates (Heemsbergen
et al. 2004), and litters of different qualities (Wardle et al. 1997a; Quested et al.
2005). Such approaches have the potential to assist our understanding of how
ecosystems may be affected by gains (through invasion) or losses (through
extinction) of species, especially if these gains or losses involve shifts in the
range of trait values in the community. However, as highlighted in Chapter 5, our
knowledge of how species losses in real communities affect ecosystem function-
ing remains limited, largely because most studies on this issue have relied on a
single approach which involves assembling artificial communities in which
organism diversity is experimentally varied, often by drawing random assem-
blages of species from a pool of species (Wardle and Jonsson 2010). We argue in
Chapter 5 that alternative approaches based on understanding which functional
traits affect ecosystem processes, and whether these traits also predispose species
to being lost from a community, represent a more fruitful and direct means for
understanding how biodiversity loss in real ecosystems influences ecosystem
functioning.
 6.3 Drivers of variability • 217

6.3 Drivers of spatial and temporal variability

6.3.1 Drivers of variation over time
Relationships between the aboveground and belowground subsystems operate over
a spectrum of temporal scales, ranging from days to seasons to centuries and
ultimately to millions of years. Those which occur over the shortest timescales
(days to years) often involve temporal variation in resource availability (Bardgett
et al. 2005). For example, in Chapter 2 we emphasized through examples in alpine
ecosystems that seasonal dynamics of the soil microbial community can drive
temporal patterns of nutrient availability for plants, leading to microbes and plants
partitioning nutrients across seasons. Further, as discussed in Chapter 4, foliar
herbivory can lead to a pulse in root exudation, which often promotes soil micro-
bial activity and nutrient mineralization in the root zone, and ultimately benefits
plant growth. Many other examples have been reported of ephemeral resource
pulses influencing the belowground and aboveground subsystems, and these can
arise from both plants (e.g. seasonal litter fall, storm damage, mast seeding events,
pollen inputs; Chapter 3) and animals (e.g. faecal deposits and carcasses; Chapter
4). One important example described in Chapter 4 involves adult cicadas, which
emerge as adults only every 17 years. The carcasses of cicadas serve as a major
resource pulse when they die, with wide-ranging consequences both above and
below ground (Yang 2004). Despite a growing number of examples of resource pulses
in ecosystems (Yang et al. 2008), drivers of temporal variability of aboveground–
belowground linkages remain poorly understood, especially at the inter-annual
level. As such, while we know that ecosystem NPP varies greatly across years in
response to macroclimatic variation, and that the magnitude of this variation depends
on site factors such as vegetation type (Knapp and Smith 2001), much remains
unknown about how this in turn influences inter-annual variation in the belowground
subsystem or feedbacks aboveground. Further, as discussed in Chapter 4, inter-annual
variation in rainfall has been shown to drive variation in how grazing herbivores affect
plants and nutrient cycling (e.g. Augustine and McNaughton 2006), again suggesting
likely effects of inter-annual climatic variation on aboveground–belowground
linkages.
With regard to longer time-scales (decades to centuries), ecologists have long
recognized that aboveground and belowground properties change in predictable
directions during ecosystem succession and development, as discussed in Chapter 3.
While it is reasonably well understood that particular characteristics of the above-
ground and belowground subsystems often shift in parallel over successional time,
the mechanistic basis of how these subsystems interact during succession is less well
understood. However, some recent plant–soil feedback experiments in herbaceous
systems have provided evidence that negative feedbacks between early successional
plant species and their associated soil biota may hasten their replacement during
succession (e.g. De Deyn et al. 2003; Kardol et al. 2006). Further, as described in
Chapter 3, types of soil organisms that may not thrive in plant–soil feedback
218 • 6 Underlying themes and ways forward

experiments, such as mycorrhizal fungi and decomposer organisms, are also involved
in feedbacks with the plant community, which influence plant species replacement,
although this has been seldom investigated. In particular, little attention has been
given to understanding how plant species feedbacks with the decomposer subsystem
influence soil nutrient supply and availability, and ultimately vegetation change (but
see Berendse 1998; Bowman et al. 2004; Meier et al. 2008). Further, as discussed in
Chapter 5, some recent studies are beginning to provide evidence that plant–soil
feedbacks are relevant for understanding plant invasions and the extent to which
invaders may be able to dominate the plant community and replace native species
(Van der Putten et al. 2007).
It is widely recognized that foliar herbivores have important effects on vegetation
change and ecosystem succession, and that depending on context they can both
accelerate and retard plant succession. As discussed in Chapter 4, this often has
major consequences for the functional composition of vegetation, the quantity and
quality of resources that plants return to the soil, and ultimately soil properties and
nutrient availability. However, a recent and growing body of literature also highlights
the potential for herbivores to cause ecosystems to rapidly undergo large stepwise
transitions to alternative ‘stable states’; as highlighted in Chapter 4, this is especially
apparent when overgrazing has led to soil degradation and an irreversible collapse of
existing vegetation (Rietkerk et al. 1997; Rietkerk and van de Koppel 1997). In these
circumstances, mosaics of vastly contrasting patches can result, with the status of each
patch depending on whether the herbivores have driven it past a critical transition.
From Chapter 5, it is apparent that these rapid changes to alternative stable states can
also occur when functionally important herbivores either invade a new ecosystem (e.g.
invasions of beavers and subsequent tree felling in southern South America; Fig. 5.16)
or become extinct (e.g. the Pleistocene extinctions of mega-herbivores in the sub-
Arctic; Zimov et al. 1995). These types of sudden transitions have been studied mostly
from an aboveground perspective, but are also likely to have large and rapid effects on
the belowground subsystem, especially given the large changes in plant-derived
resource input and soil disturbance which they frequently involve.
Relationships also occur between aboveground and belowground communities over
much longer timescales, in the order of millennia and beyond. As outlined in Chapter 3,
in the long-term absence of catastrophic disturbance during succession, a decline or
retrogressive phase can occur which results from a prolonged decline in the availability
of nutrients (notably phosphorus), which eventually leads to declines in plant production
and biomass, litter quality, abundance of soil organisms, and decomposition and nutrient
mineralization (Vitousek 2004; Wardle et al. 2004b). This retrogressive phase often
occurs over geological timescales (e.g. 4.1 million years on the Hawai’ian islands;
Vitousek 2004) and is associated with changes in the parent material and soil that occur
during pedogenesis. Studies of ecosystem retrogression have greatly advanced our
understanding of how variation in nutrient availability at local spatial scales drives
community and ecosystem processes. However, retrogression has been compre-
hensively studied in only a few locations, and the issue of whether the phenomena
that have been identified in retrogressed ecosystems also apply to other areas containing
 6.3 Drivers of variability • 219

nutrient-depleted old soils (e.g. as occurs in much of the tropics) is poorly understood.
Before leaving this topic, the nature of relationships between the aboveground and
belowground subsystems and the consequences for ecosystem change over even more
lengthy geological and evolutionary timescales (in the order of millions of years) has
scarcely been explored. However, Berendse and Scheffer (2009) recently proposed that
the large increase in angiosperms relative to gymnosperms during the Cretaceous may
have resulted from angiosperms producing much higher-quality litter than gymno-
sperms, leading to greater nutrient supply rates in the soil. This in turn set a positive
feedback in motion, leading to a rapid increase in angiosperms (and eventually angio-
sperm dominance) once they had reached a critical density.

6.3.2 Drivers of variation over space

Variability in aboveground and belowground properties of terrestrial ecosystems
occurs across a very broad spectrum of spatial scales (Ettema and Wardle 2002)
(Fig. 3.4). Such spatial variation occurs in a nested structure and is driven by a
hierarchy of extrinsic and intrinsic factors, leading to patterns of spatial aggregation
ranging from square millimetres to hectares (Ettema and Wardle 2002). For example,
at large spatial scales, topographic variability has an important role in determining
heterogeneity of resources such as soil nutrients and moisture, as well as soil structure,
which in turn drives the spatial variability of plants, soil biota, and aboveground
consumers. Nested within this at local scales, spatial variability in both the above-
ground and belowground subsystems is driven by patchiness of vegetation and
activities of larger bodied aboveground and belowground fauna. At the finest
spatial scale, spatial variability in microtopography and soil porosity, as well as the spatial
arrangement of litter fragments and soil organic matter hotspots, determines the spatial
distribution of small-bodied soil organisms such as microbes, nematodes, protozoa,
and microarthropods, as well as the decomposition and mineralization processes that
they drive. A recurrent theme throughout this book has been the elucidation of how
plants, soil organisms, and herbivores can contribute to spatial variability on both
sides of the aboveground–belowground interface, and the consequences of this
variability for community- and ecosystem-level processes and properties.
As outlined in Chapter 3, coexisting plant species can differ greatly in their key
traits, including those that are important in driving belowground communities and
their activity. When individuals of different coexisting species (or even different
coexisting genotypes within species) are spatially segregated, and when horizontal
transport of plant-derived resources is low, then each individual plant has the
potential to strongly affect the soil beneath it. When these coexisting plants differ
greatly in terms of their belowground effects (e.g. in terms of their litter quality and
rhizosphere influences) then this can be a powerful driver of spatial heterogeneity of
soil organisms, decomposer processes, and nutrient supply rates from the soil. At its
most extreme, this can lead to individual plants creating ‘islands of fertility’ and ‘tree
islands’, as discussed in Chapter 3. What remains less well understood is how these
individual plant effects on belowground spatial variability feedback aboveground,
220 • 6 Underlying themes and ways forward

although these effects can conceivably be either positive or negative. As an example

of a negative effect, individual plants can promote pathogens in the patches that they
occupy, adversely influencing their success, as has been shown for Prunus serotina
by Packer and Clay (2000). This could in turn reduce or promote spatial variability of
the belowground subsystem, depending on what effect that species has on below-
ground patchiness. As an example of a positive effect, each individual plant in a
multispecies community may control belowground resource availability in the patch
that it occupies, with all species potentially being maintained in their own patches.
This would in turn maintain vegetation heterogeneity and, potentially, plant species
diversity. Although there is theoretical support for such a mechanism (e.g. Huston
and De Angelis 1994), direct experimental evidence for it is scarce. However, the
ability of some coexisting tree species to select for decomposer communities that
preferentially break down (and presumably mineralize) their own litter (Vivanco and
Austin 2008) provides some support for this idea. Further knowledge of the mech-
anisms of how aboveground–belowground feedbacks may contribute or respond to
plant patchiness may help our understanding of the factors that structure plant
communities and influence interactions involving invasive and range-expanding
plant species, as considered in Chapter 5.
Consumer organisms may be an important driver of spatial variability both above-
ground and belowground, especially when they drive the spatial redistribution of
resources. As we revealed through several examples in Chapter 2, belowground
invertebrates can greatly promote spatial heterogeneity at a range of scales, deter-
mined in part by animal body size. Detritivorous microarthropods promote hetero-
geneity at very local spatial scales by producing faecal pellets that serve as hotspots
for microbial activity and nutrient release. At larger scales, earthworms form casts
and middens that influence microbes and smaller-bodied soil organisms, and in
grasslands promote the establishment of some plant species over others. Social soil
animals such as termites and ants concentrate resources into the nests that they
construct, which in turn eventually become colonized by some plant species and
not others, often contributing to vegetation heterogeneity in the landscape and driving
plant succession Further, as discussed in Chapter 4, aboveground animals, notably
grazing herbivores, can contribute greatly to belowground and vegetation heterogen-
eity, through patchy returns of resources such as dung and urine (e.g. Schütz et al.
2006; Jewell et al. 2007), and even their carcasses (e.g. Bump et al. 2009a, 2009c;
Parmenter and MacMahon 2009). An important development is the recognition that
herbivores can also promote landscape heterogeneity through causing alternative
stable states of vegetation, leading to vegetation mosaics (Rietkerk et al. 1997;
Rietkerk and van de Koppel 1997). However, most studies on this issue have focused
above ground, and the consequences for belowground organisms and processes have
been seldom explored. Further, a number of studies have highlighted the ability of
consumer organisms to reorganize the spatial distribution of resources in the landscape,
either through consuming resources in one part of the landscape and depositing them
elsewhere, or through moving resources across ecosystem boundaries such as
from aquatic to terrestrial. Finally, as highlighted in Chapter 5, ecosystems may be
 6.3 Drivers of variability • 221

subjected to particularly significant transformations when animals that drive the

redistribution of resources are either lost from the ecosystem or invade it. For
example, invasive predators of seabirds that thwart the transfer of resources by
these birds from the ocean to land can cause spectacular transformations in both
aboveground and belowground properties, and the functioning of the ecosystem (e.g.
Fukami et al. 2006; Maron et al. 2006).

6.3.3 Differences across ecosystems

Much of the material in this book has focused on comparisons among contrasting
ecosystems. Ecosystems can vary greatly even over small geographic scales, as a
result of fundamental differences in either soil fertility (driven by parent material and
abiotic soil properties) or macroclimate, although at local spatial scales more atten-
tion has focused on the former. As such, there are widely recognized fundamental
biotic differences between fertile and infertile ecosystems that are driven by soil
properties and fertility (Fig. 4.3). As discussed in Chapter 3, fertile habitats are
dominated by plant species that are adapted for rapid resource acquisition rather
than resource conservation, and also produce litter that is of much lower quality when
compared with plant species characteristic of infertile habitats. Further, as we de-
scribe in Chapter 2, fertile habitats favour bacterial-based food webs that promote
rapid cycling of nutrients, rather than fungal-based food webs that are more adapted
for conserving nutrients. And, as outlined in Chapter 4, herbivores consume a much
higher proportion of total plant productivity in fertile than in infertile systems, and are
likely to retard rather than promote plant succession. As such, in infertile ecosystems,
plants, decomposers, and herbivores will interact in such a way as to enhance nutrient
retention and conservation of limiting nutrients, while in fertile systems these groups
tend to interact in a manner that promotes rapid nutrient acquisition and use. As
emphasized through numerous examples throughout this book, interactions between
these three groups of organisms involve a range of feedback mechanisms which both
positive and negative outcomes for both aboveground and belowground ecosystem
processes. Much remains to be discovered, however, about how these feedback
mechanisms vary between fertile and infertile ecosystems, or how they may them-
selves enhance or reduce soil fertility.
A key element of how ecosystems differ involves ‘context dependency’ of species
effects on community and ecosystem properties. While much research has focused on
how species affect ecosystems, greater emphasis is now focusing on how these effects
can be driven by environmental context. As noted in Chapter 2, soil animals can vary
greatly in their effects on microbes and decomposer processes depending on what
habitat they are in. For example, the indirect effect of spiders on decomposition can
depend on habitat moisture regime (Lensing and Wise 2006), and the indirect effect
of predatory mites on soil microflora depends on soil fertility (Lenoir et al. 2007).
Similarly, as outlined in Chapter 4, foliar herbivores can indirectly influence below-
ground biota and processes through a range of mechanisms, some positive and some
negative. Different mechanisms dominate in different contexts, for instance along
222 • 6 Underlying themes and ways forward

gradients of soil fertility or topography, and herbivores can therefore have either net
positive or negative effects depending on which ecosystem or part of an ecosystem
they are in. The nature of plant–soil feedbacks may also be context-dependent, and as
outlined in Chapter 5 the magnitude and even the direction of feedback that some
invasive plant species have with their associated soil biota depends on whether they
are growing in their native range or in a newly invaded area. The issue of context
dependency has also arisen in the literature of how changes in biodiversity affect the
functioning of ecosystems; as discussed in Chapter 5, a growing number of studies
show that environmental factors that differ across ecosystems helps determine
whether and how community diversity of plants and their consumers may affect
key aboveground and belowground processes. One of the challenges in studying the
ecology of aboveground–belowground relationships continues to be to understand
not just the basis through which species affect community and ecosystem properties,
but also how and why these effects may differ in different environmental contexts and
across contrasting ecosystems.
Other attributes that characterize differences among ecosystems are ratios of major
nutrients (Elser et al. 2000). As outlined in Chapter 3, the nitrogen-to-phosphorus
ratio of ecosystem components, such as plants, microbes, animals, and soil organic
materials, are linked and have the potential to vary greatly across ecosystems. For
example, ecosystems that have undergone retrogression have much lower availability
of phosphorus relative to nitrogen than those that have not. This diminished avail-
ability of phosphorus greatly elevates the nitrogen-to-phosphorus ratio of biological
tissues, and leads to reduced plant productivity, and rates of decomposition and
nutrient supply from the soil (Wardle et al. 2004b). Additional changes include
increased domination of the fungal-based relative to the bacterial-based energy
channel, and reductions in the abundance of most groups of soil invertebrates. Recent
work by Mulder and Elser (2009) and Reuman et al. (2009) also provides strong
evidence for community-level effects of variation in nitrogen-to-phosphorus ratios
in soil food webs in Dutch agricultural fields. Here, increases in soil nitrogen-to-
phosphorus ratios across fields alter the allometric slope between faunal abundance
and body size, in part through favouring small-bodied organisms associated with
the bacterial-based energy channel at the expense of larger-bodied organisms
associated with the fungal-based energy channel. As is apparent through Chapter
2, this should in turn have important implications for differences across ecosystems
in soil nutrient cycling, and feedbacks aboveground. However, studies of how
variation in the nitrogen-to-phosphorus ratio across ecosystems affects community
and ecosystem properties are still few, and much remains unknown about how this
ratio drives interactions between decomposers, plants, and their consumers.

6.3.4 Global-scale contrasts

As is apparent in the preceding chapters, aboveground and belowground biota, and
the processes that they drive, vary greatly among biomes and therefore at the sub-
global to global scale. Variation in major groups of soil biota at the global scale has
 6.3 Drivers of variability • 223

been characterized by various authors, both qualitatively (e.g. Swift et al. 1979)
and quantitatively (e.g. Wardle 1992; Fierer et al. 2009). These is also some
recognition that the functional capabilities and importance of major groups of
soil organisms varies greatly across different climatic zones; for example, earth-
worm species from lower latitudes have the enzymatic capability to digest more
recalcitrant substrates than do those from higher latitudes (Lavelle et al. 1995). As
such, while we have a reasonable knowledge as to how the main groups of soil
biota vary sub-globally or globally, there have been few robust tests of how the
different components of the soil biota vary in their functional role at these broad
scales, or the consequences of this for ecosystem processes and interactions
between the aboveground and belowground subsystems. However, some recent
studies have utilized a manipulative approach to investigate the role of soil fauna in
driving litter decomposition across ecosystems at these larger scales (e.g. Gonzalez
and Seastedt 2001; Wall et al. 2008; Powers et al. 2009). These have involved
placement of litter bags in combination with treatments to allow or exclude access
by decomposer fauna, and with findings being interpreted in terms of the inter-
active effects of fauna and macroclimate (temperature and/or precipitation) on rates
of decomposition.
One major issue that has attracted surprisingly little attention is the relative role of
macroclimate versus soil fertility in explaining sub-global- or global-scale variation
in belowground and aboveground biota, or the ecosystem processes that they drive.
This is reflective of the macroecological literature in general, which has often paid
scant attention to soil properties and/or soil fertility as a driver of patterns at these
scales (but see Huston 1993). Tropical soils are generally less fertile than those at
higher latitudes, because they are more depleted in organic matter, and are much
older, more weathered, and contain less phosphorus. Therefore, at a global scale,
macroclimate and soil fertility are not independent, and as such there are problems in
determining whether climate drives sub-global or global variation of organisms and
processes directly (through direct effects of temperature and precipitation) or indir-
ectly (via long-term effects on soil fertility). However, studies at the sub-global to
global scale suggest that both are probably important. For example, soil fertility has
shown to play an important role in explaining variation among biomes in soil biota
(Wardle 1992; Fierer et al. 2009), and macroclimatic variables serve as useful
predictors of both the rate of litter decomposition (Berg et al. 1993) and the role of
soil animals in driving decomposition at sub-global scales (Wall et al. 2008). How-
ever, some variables may be driven much more by soil fertility than by climate. For
example, a recent analysis by Huston and Wolverton (2009) provides compelling
evidence that global variation in NPP in forests is driven largely by soil fertility rather
than temperature, with tropical forests on average being less productive than temper-
ate ones because they grow on less fertile soils. This has important implications for
the belowground subsystem, which as discussed in Chapter 3 is driven in part by
ecosystem productivity. Further, Cornwell et al. (2008) provided evidence that local
variation in plant traits, which is likely to be driven primarily by soil fertility, is a
more powerful determinant of rates of litter decomposition than is sub-global to
224 • 6 Underlying themes and ways forward

global variation in macroclimate. However, direct evidence about the role of macro-
climate versus soil fertility in explaining global variation in aboveground or below-
ground biota and the processes they drive remains scarce.

6.4 Global change phenomena

A topic that we have emphasized throughout this book involves the impact of human-
induced global change (including carbon dioxide enrichment, climate change, nitrogen
deposition, invasion of alien species into new territories, and losses of native species) on
aboveground and belowground biota and the processes that they drive. Moreover, we
have illustrated how these effects of global change can have far-reaching consequences
for ecosystem-level properties and feedbacks to the Earth-system. One important
development in this area has been the recognition that global change phenomena have
both direct and indirect effects on the belowground subsystem, and that such effects
create feedbacks that influence aboveground biota, ecosystem nutrient and carbon
cycling, and the flux of carbon dioxide and other greenhouse gases from land to
the atmosphere. This understanding is perhaps most developed in the context of
climate change and its consequences for ecosystem carbon dynamics and carbon-
cycle feedbacks. For example, as detailed in Chapters 2 and 3, many examples now
exist in the literature showing that climate change can impact directly on soil organisms
and ecosystem carbon cycling through changes in temperature and precipitation, and
extreme climatic events, and indirectly via climate-driven changes in plant productivity
and community composition. This in turn alters soil physicochemical conditions, the
supply of carbon to soil, and the structure and activity of soil communities involved in
decomposition processes and carbon loss from soil (Fig. 2.19). Likewise, much litera-
ture exists demonstrating that nitrogen enrichment, which has increased substantially as
a result of anthropogenic activity, can significantly affect the belowground subsystem
and ecosystem-level processes through strong direct effects on soil organisms and
through indirect effects on vegetation change.
Although understanding in these areas has increased dramatically in recent years,
significant gaps nevertheless remain. For instance, very little is known about the
relative contributions of direct and indirect effects of global change phenomena on
ecosystem properties, although recent manipulative experiments are beginning to
shed light on this issue (e.g. Manning et al. 2006; Suding et al. 2008). Also, there are
considerable gaps in our understanding of the response of soil respiration to climate
change, which in part stems from the fact that it is regulated by a myriad of factors,
including resource quality (Davidson and Janssens 2006) and a variety of interactions
and feedbacks between climate, plants, their herbivores and symbionts, and free-living
soil organisms (Wolters et al. 2000; Högberg and Read 2006; Bardgett et al. 2008).
Moreover, very little is known about the consequences of extreme events associated
with climate change, such as droughts and soil freezing, for aboveground and below-
ground biota and ecosystem processes, or of the role that simultaneous global change
drivers play in regulating community and ecosystem-level processes. Indeed, as
 6.4 Global change phenomena • 225

highlighted in Chapters 2 and 3, it is becoming increasingly apparent that our ability

to predict future responses to global change requires a greater understanding of the
simultaneous effects of multiple global change drivers on soil biological communities
(Bardgett et al. 2008; Tylianakis et al. 2008). As we illustrate in Chapter 2, there is
much potential for interactions between global change drivers to amplify, suppress or
even neutralize climate change driven effects on the belowground subsystem and
their feedback to carbon exchange. Studies in this area are still few, and we therefore
suggest that experiments which simultaneously vary two or more global change
drivers offer much promise for improving our understanding of how aboveground–
belowground interactions and their influence on ecosystem-level processes may
respond to current global change scenarios. This represents a major research chal-
lenge for the future.
An important but rarely considered issue that emerges from this book is that
aboveground consumers have the potential to significantly alter the impacts of global
change on the functioning of terrestrial ecosystems. One important development in
this topic is the recent recognition that aboveground herbivores not only strongly
affect net ecosystem carbon exchange (e.g. Welker et al. 2004; Ward et al. 2007; Van
der Wal et al. 2007), and hence the source–sink activity of terrestrial ecosystems, but
they can also alter the influence of climate itself on land–atmosphere carbon fluxes
(Polley et al. 2008). Moreover, recent experimental studies are beginning to show that
grazing can strongly modulate the effects of climate change on the carbon balance of
terrestrial ecosystems. For example, studies in the Arctic point to interactive effects of
warming and grazing on plant community composition (Post and Pedersen 2008),
belowground processes (Rinnan et al. 2009) and ecosystem carbon-sink strength
(Sjögersten et al. 2008). Further, evidence from long-term studies suggest that
woody plant expansion in response to warming is able to be constrained by large
herbivores (Post et al. 1999; Olofsson et al. 2009). As we stress in Chapter 4, much
remains to be learned about the response of herbivores (and other trophic groups such
as predators) to climate change and the consequences of this for community- and
ecosystem-level processes, including ecosystem carbon exchange and carbon-cycle
feedbacks. Given the dearth of studies in this area, we maintain that there is a
significant need for more research aimed at an improved understanding of how
herbivores, and other biotic factors, modulate ecosystem responses to climate change,
and ultimately how herbivore management might be altered to mitigate climate
change. Such research is especially important given the need for predictive models
to accommodate biotic factors such as grazing in order to accurately simulate carbon
dynamics in terrestrial ecosystems.
As we highlight in Chapter 5, global climate change is an important driver of
species gains and losses in ecosystems, with potentially far reaching consequences
for aboveground and belowground properties of ecosystems, and climate feedbacks.
An issue that we highlight in Chapter 5 involves invasive and range-expanding
species, and their potential to influence community- and ecosystem-properties
properties. Indeed, evidence is now mounting that species range shifts are wide-
spread across taxonomic groups and geographic regions (e.g. Hickling et al. 2006;
226 • 6 Underlying themes and ways forward

Menendez et al. 2007; Lenoir et al. 2008), and that climate warming plays
a significant role in these shifts (Walther et al. 2002; Parmesan and Yohe 2003).
Although a relatively understudied topic, there is now mounting evidence that range
shifts can have important effects on ecosystem properties and potentially on carbon-
cycle feedbacks (e.g. Knapp et al. 2008; Kurz et al. 2008; Takatsuki 2009), and that
range-expanding species may differ from related native species in the nature of their
interactions with their antagonists in their new or expanded range (Engelkes et al.
2008). However, as we highlight in Chapter 5, it is apparent that the scale of impacts
of range-expanding species will vary greatly depending on many factors, including
the traits of those species that are shifting in their range and the environmental
characteristics of the habitats into which they invade, which may also be affected
by climate change. A major challenge for the future, therefore, will be to understand
the mechanisms by which climate change simultaneously impacts on terrestrial
ecosystems through range shifts and through its direct and indirect effects on resident
aboveground and belowground communities.
As we highlighted at the start of this book, the aboveground and belowground
components of ecosystems have traditionally often been considered in isolation from
one another. However, as illustrated in this book, the last two decades, and especially
the last 5 years, have witnessed a proliferation of studies that have explored the
influence that these components exert on each other, and the role that aboveground–
belowground interactions play in controlling the structure and functioning of terres-
trial ecosystems and their interactions with drivers of global change. This recent
activity has led to major advances in the field of ecosystem ecology, especially
through demonstrating the over-riding role that organism traits and biotic inter-
actions, both among and within trophic levels and on both sides on the above-
ground–belowground interface, play as terrestrial ecosystem drivers. Moreover, we
now know much more about the role that aboveground–belowground interactions
have in regulating ecosystem responses to global change, and in controlling carbon-
cycle feedbacks with consequences for the Earth-system. However, as we highlight
throughout this book, many challenges remain, and most notably there is a significant
need to use our advancing knowledge of aboveground–belowground interactions to
improve their representation in current concepts relating to global-scale patterns and
processes. Indeed, while many detailed empirical studies have been carried out on
different types of aboveground–belowground interactions, we still lack a strong and
unifying theoretical basis for the subject, and this limits our ability to make predic-
tions about their role in regulating terrestrial ecosystem processes and their response
to global change. Likewise, while our understanding of plant and soil microbial
processes involved in carbon cycling has advanced greatly, this is not well repre-
sented in global carbon models. Finally, the science of ecosystem ecology is becom-
ing increasingly directed towards understanding and predicting the effects of global
environmental change on the delivery of ecosystem services upon which humans
depend. This approach presents many new challenges for ecosystem ecologists,
including the need to better understand the role of aboveground–belowground inter-
actions as drivers of ecosystem services and human well-being.
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Index

Abies balsamea 139 antagonistic plant–soil relationships 86, 87

abiotic factors and plant communities 90
litter loss 104 soil biota–host plants 16
plant decomposition 46 Antarctica 54, 55
aboveground communities ants
decomposers, effects of 17–28 carbon concentration in nests 47
interactions with soil organisms 16 in decomposition 47
NPP and shrub expansion 205 as ecosystem engineers 45
aboveground–belowground interactions invasive species 194–5, 199
as ecosystem drivers 7, 8–10 mound-building 43
global change in 10–12 spatial variability, drivers of 220
long time-scales 217–18 and vegetation dynamics 42–4
non-nutritional links 8 see also leaf-cutter ants
acceleration/deceleration model 117, 154, 155 aphids
Adelges tsugae 195 diversity, importance of 171
agriculture in trophic cascades 139–40
land use changes 57–8 Aporrectodea longa 41
livestock movement 142–3 arbuscular mycorrhizal fungi
multiple species cropping 72 and invasion 189
allelochemical compounds 188–9 nitrogen transfer 33–4
Alliaria petiolata 189 and plant community dynamics 9, 36, 37
allocation 121–2, 136 and plant traits 76
Alnus spp. 32, 33, 34, 86 plants dependent on 189
alpine ecosystems Arctic ecosystems
and climate change 56–7, 102, 104, 106, 201 alternative stable states 132–4
microbial nitrogen 23 and climate change 56–7, 61, 102, 104, 106,
seasonal dynamics 21 202
tundra plants 18 herbivory on carbon fluxes, effects of 158–60
alternative stable states 218 microbial nitrogen 23
herbivory-induced 132–4 plant functional type changes 103
invasion-induced 201 reindeer grazing, effects of 120
Amanita spp. 191 tundra plants, nitrogen uptake in 18, 20
amino acid uptake 18–19 Arjeplog (Sweden) chronosequence 93, 95
ammonium oxidizers 23 Armillaria luteobubalina 191
Ammophila arenaria 87, 171 Arthurdendyus triangulata 193, 194
animal wastes, aboveground 114
invertebrate 119–20 bacteria
livestock movement 142–3 growth control 32
and nutrient cycling 117–19 species in soil 15
plants, effects on 122 diversity, importance of 170–1
290 • Index

bacteria (cont.) carbon cycle

see also cyanobacteria; nitrogen-fixing bacteria; and soil 45–59
soil fungal:bacterial ratio soil organic carbon 45, 46
bacterial energy channels 28–32, 60 in climate change 106
bacterial growth and nutrient availability 32 carbon-cycle feedbacks 4, 60
C:N ratio 28, 29, 30 and climate change 52–7
and land use changes 57–8 carbon dioxide
and nitrogen enrichment 108 belowground–atmosphere movement 45–6
batatasin III 66, 67 exchange with atmosphere 154–5
bears 150 free-air carbon dioxide (FACE)
beavers 128, 196, 198 experiments 100
Betula nana 160 nitrogen cycle, effects on 12
Betula pendula rising concentrations 99, 101, 102
decomposer diversity, effects of 169 soil organisms, impact on 11, 48
plant–soil fauna mutualism 87–8 sources 45–6
soil fauna, effects of 8 see also net ecosystem exchange
spatial distribution 71 carbon dynamics
within-species variability 68, 69 aboveground consumers and global
Betula pubescens 124, 126 change 152–61
biodiversity exchange
belowground effects, temporal 171 autotrophic/heterotrophic effects 50, 51–2
and climate change 101 and climate change 100
as ecosystem drivers 7 ecosystem processes 46–52
and ecosystem processes 166–7 fluxes
magnitude of effects 173 and climate change 158–60
and herbivory 39 and herbivores 158–60
loss, factors affecting 10 herbivores, influence of 153
mycorrhizal fungi in 37–8 land–atmosphere 158
and net primary production 167, 171 from plant roots 100
and soil pathogens 38 and herbivore range expansion 204, 206, 207
and soil respiration 48 carbon mineralization
species loss through extinction 166–72 and climate change 55
biological soil crusts 35 earthworms in 47
bird range changes 202 soil fauna in 50, 51
bison carbon sequestration traits 106–7
exclusion experiments 115, 179 caribou 207
extinction, effects of 181 Carmichaelia odorata 33, 86
grazing, effects of 119 Castanea dentata 195
and nitrogen cycling 144 Casuarina spp. 32
Bouteloua gracilis 8 cattle
Briza media 143 grazing, effects of 118
Bromus tectorum 186 nutrient redistribution 143
bryophytes Centaurea maculosa 189
as ecological drivers 215 cervids see deer; elk; moose
plant trait–soil biota interaction 79, 80 chironomids 151
Buddleja davidii 83 chronosequences 3
ecosystem retrogression 93–4, 95, 96
Calluna vulgaris 5, 62 cicadas 145, 147
Campanulastrum americanum 145 climactic gradients 3
canopy gap formation 93 climate change
carabid beetles, invasive 194–5 belowground effects 99–107, 226
carbon see soil carbon and carbon dioxide increases 99
 Index • 291

and carbon fluxes 158–60 aboveground effects 169–71

causing species loss 201 ecosystem, effects on 17–32, 87
and decomposition 11 in litter-mixture experiments 169
drivers, multiple 57–9 litter N:P ratios, effects of 84–5
feedbacks 45, 46 selection by plants 64, 89, 90, 203, 212–13
and herbivory 152–61 decomposition
vegetation composition effects 160–1 abiotic factors 46
plant communities, effects on 160 and climate change 11, 53–5
positive feedbacks 11 in ecosystem retrogression 96, 97
range-expanding species 12, 226 of herbivore carcasses 145
and soil carbon dynamics 13 of invertebrates 145
and soil fertility 223–4 microbial predation, effects of 25
and soil organisms 52–7 of peat, multiple factors in 57
and species losses/gains 201, 225 and shrub expansion 103
see also global warming; temperature soil biotic interactions 46
collembolans across ecosystems 50
abundance and species richness 69 soil macrofauna in 47
collembolan grazing, effects of 48 and trophic cascades 48
effects of herbivory on 128, 129 predator-induced 27
grazing activities, effects of 52 see also litter decomposition
communities see aboveground communities; plant deer
communities carcasses as resources 145
community ecology 4 exclusion experiments 115, 196, 197
community heritability 70 invasive species 195–6
Congettia sphagnetorum 25–6 and predators 139, 181
consumers, aboveground range changes 207
carbon dynamics and global change 152–61 selective feeding effects 123, 124, 125, 126
ecosystem, effects on 113–64 defoliation
ecosystem-level significance 113–64, 225 mycorrhizal fungi, effects on 127
invasion by 195–201 plants, effects on 121, 122
spatial movement of resources 141–51 Dendrobaena octaedra 192
across land 142–7 Dendroctonus ponderosae 204, 206–7
aquatic to terrestrial ecosystems 142, 147–51 denitrification 23
see also herbivores Deschampsia spp. 66, 67, 109–10, 176
Coolcoola (Queensland) chronosequence 93, 94, desertification 128, 204
95 disturbance
Coriaria arborea 34, 83 by herbivores 114, 122, 127–30
cougars 138, 181 spatial/temporal localization 130
crabs 199 and spatial patterning of soil biota 70
Cryphonectria parasitica 195 and vegetation succession 90–9
Cubitermes severus 41 drought
cyanobacteria peatlands, effects on 56
nitrogen-fixing 9, 34, 35 soil microbes, effects on 55–6
in species removal experiments 176 dung beetles 41
in decomposition 47
Dacrydium cupressinum 176 and vegetation dynamics 44–5
decomposer food webs 18, 26 dynamic global vegetation models (DGVMs) 4
and net primary production 64, 65
predators, effects of 141 Earth-system science 3, 4
decomposers earthworms
decomposer–plant relationship 88 casts 41
diversity, effects of 169, 170 in decomposition 47
292 • Index

earthworms (cont.) plant communities, effects of 7

as ecosystem engineers 40–2, 45 plant traits, effects of 81, 84–5
invasive 192 range changes 201–2
conceptual model of effects 193 retrogression 93–7, 218–19
multiple plant species, effects of 74 and root-associated biota 32–8
and plant productivity 25 species diversity, effects of 7
and plant traits 76 stability 171
predation by invasive species 193, 194 stoichiometry and plant traits 84–5
removal experiments 178 strategy-based theory 3
role of 15 and termites 42
and soil structure 45 ectomycorrhizal fungi 76
spatial variability, drivers of 220 and invasion 189, 191
and vegetation dynamics 41–2 and plant community dynamics 36–7, 38
ecosystem engineers 40–5 and plant traits 76
ecosystem goods/services 13–14 plants dependent on 189
ecosystem processes elk
aboveground consumers 113–64 exclusion experiments 115
and ants 42–4 grazing, effects of 119, 144
belowground interactions 15–61 and nitrogen cycling 144
and biodiversity 171 and predators 139, 181
magnitude of effects 173 Empetrum hermaphroditum 66–7
biodiversity variations, effects of 166–7 enchytraeids 25–6, 74, 76, 128
biotic interactions in 4 enzymes excreted by ectomycorrhizal fungi 36
carbon exchange 46–52 Erica tetralix 66, 88, 98
and climate change 201 ericoid mycorrhizal fungi 76
‘context dependency’ 221–2 exclusion experiments 115, 179, 196, 197
decomposers, effects of 17–32 extinctions
drivers aboveground–belowground perspective 166–72
aboveground–belowground interactions 8–10 ecological effects 166, 181–3
differences across ecosystems 221–2 experimental approaches 180
global scale contrasts 222–4 human-induced factors 165
plant species 62 megaherbivore populations 166, 181, 182, 196
spatial variability 219–21 non-random 173
species/biotic interactions 5–8 in real ecosystems 179–83
temporal variability 217–19 removal experiments 172–9
and dung beetles 44–5 species losses through 166–83
and earthworms 41–2 aboveground–belowground
extinction, effects of 13, 166–83 perspective 166–72
large organisms 182–3 in real ecosystems 180–3
through human activity 179–80, 181 removal experiments 172–80
feedback controls 15 species traits in 180–1
herbivory and plant–soil feedbacks 114–34
landscape-scale effects 130–2 facilitation interactions 90–1
multiple stable states 132–4 farming intensification 57–8
negative belowground effects 123–30 feedback systems 3–4
positive belowground effects 116–23 aboveground–belowground biota 62
historical perspective 3–5 controlling ecosystem 15
invasion, effects of 13, 183–201 ecosystem–plant functional type 103
transformation 198, 201, 221 herbivory–nutrient cycling 124–5
landscape-scale effects 130–2, 196, 220 mycorrhizal fungi in 218
nitrogen-fixing bacteria, effects of 9 plant palatability in 7
nutrient ratios, effects of 222 plant–decomposer 218
 Index • 293

and vegetation succession 98–9 fungal hyphae 15

plant–soil 10, 85–90 fungal traits 216
direct/indirect 86 fungi
experiments 85–6, 97–8 growth control 32
herbivory, effects of 117 see also soil fungal:bacterial ratio
landscape-scale effects 130–2
multiple stable states 132–4 gazelle 119, 144
negative soil/ecosystem effects 123–30 geese
positive soil/ecosystem effects 116–23 grubbing, effects of 128, 130
invasive plants 187–90 on carbon fluxes 158–60
net effects 88–90 on soil carbon/NEE 157
and plant communities 90 selective feeding effects 123
studies, drawbacks to 90 genes, plant
and vegetation succession 90, 97–9, 217 soil microbes, effects on 68, 70
plant–soil antagonist 9–10 within-species variability 68
study methodology 212 magnitude of effect 69
ferns 79, 80, 215 Geum (Acomastylis) rossii 67, 109, 110, 176
Festuca spp. 67, 143 Glacier Bay chronosequence 95
fire global change
damage and succession 93 aboveground consumers and carbon
invasive plants, effects of 187 dynamics 152–61, 225
and nutrient availability 42–3 in aboveground–belowground
promotion in climate change 105 interactions 10–12
foliage palatability 134–5, 136 belowground effects 99–110, 224
and acquisitive strategy 7 due to climate change 99–107
Folsomia candida 48 due to nitrogen deposition 107–10
food webs biotic interchange 165
detritus food webs 16 drivers 99
energy channels ecosystem, direct vs indirect effects on 224
bacterial/fungal-based 28–32 phenomena 224–6
functions 28 and soil biotic interactions 45–59
see also decomposer food webs; soil food web multiple drivers 57–9, 61
forest ecosystems global circulation models (GCMs) 4
damage and succession 93 Global Litter Invertebrate Decomposition
dominant species loss 176 Experiment (GLIDE) 51
nitrogen cycling 9, 34–5 global warming
nitrogen levels 19 and carbon dioxide 45–6, 154–5
nitrogen uptake 19 and soil respiration 52–4
Formica spp. 43–4 see also climate change
foxes, invasive 199 goats 195–6
Frankia spp. 189–90 grasses
Franz Josef glacier (New Zealand) earthworms, effects of 41–2
chronosequence 93, 95, 96 root exudates 67
free-air carbon dioxide (FACE) experiments 100 grasslands
freeze–thaw cycling/events 56 grazing, effects of 116
freezing and effects on soil microbes 55 herbivore wastes, effects of 118–19, 144
functional dissimilarity 48, 49 megaherbivore extinction, effects of 182
functional redundancy 48 nitrogen levels 19
fungal energy channels 28–32, 60 nitrogen uptake 19, 22
C:N ratio 28, 29, 30 respiration and carbon availability 156
fungal growth and nutrient availability 32 soil fauna, effects of 25
and nitrogen enrichment 108 soil food web 24, 26
294 • Index

greenhouse gases and soil 45 landscape-scale effects 114, 115, 130–2, 220
growth-promoting hormones 8 negative effects on soil/ecosystem 123–30
grubbing 128, 130, 157, 158–60 positive effects on soil/ecosystem 116–23
and resource pulses 119, 121
hares 123 and responses of plants to warming 160
Hawai’i chronosequence 93, 95 and root biomass 155
herbivores root herbivory 39–40, 87
and carbon fluxes 153, 158 selective feeding effects 113–14, 123–6
diversity, importance of 166 and soil properties 114
effects belowground 171 spatial/temporal variability of effects 131
exclusion experiments 115, 179 and vegetation dynamics 39–40
extinction of megaherbivore populations 166, Hippophae spp. 32, 33
181, 182, 196 horses 143
and global change 152 Hunt’s soil food web model 24, 26
interaction with plants 6–7, 9–10
as carcasses 145 invasive species 12, 183
invasive species 12, 128, 195 aboveground consumers 195–201
ecosystem, impact on 128, 196, 197 belowground effects 199, 201
invertebrate, as carcasses 145 belowground invaders 190–5
physical disturbance by 114, 122, 127–30 capabilities 199
and predators 7, 137, 138–9 ecosystem transformation 198, 201, 221
range changes herbivores 12
insects 204, 206–7 nitrogen-fixing 33, 199
mammals 207 plant removal experiments 81
and resource heterogeneity 144–5 plants 183–90
and soil carbon stores 152–4 coexisting species, effects on 188–9
vertebrate ecosystem, effects on 187
invasive species 195–6 factors influencing 190
loss of 166, 179, 181, 182 and fire 187
herbivory plant–soil feedbacks 187–90
belowground effects 122–3 range/abundance 190
and body-size 131–2 and root-associated biota 12
carbon/nitrogen allocation, effects on 121–2 species gains 183–201
ecosystem, effects on 9–10 vs native species 166, 183–7
foliage/litter quality, effects on 113 invertebrates 145
foliar 218 herbivores/herbivory
invertebrate 119–20 predators, effects of 139–40
predators, effects of 139–40 wastes, effects of 119–20
mycorrhizal fungi, effects on 127 nutrient transfer
and NEE 155–7, 158 by decomposition 145
and nutrient cycling 116–20 freshwater to land 149–51
spatial distribution 119 range changes 202
overgrazing 128, 132 ‘islands of fertility’ 71, 204, 219
and plant traits 6–7, 118, 134–7
belowground processes in 136–7 land use changes 57
favoured by grazing 135, 136 Lasius flavus 44
models 134–5 leaching 45
and plant–soil feedbacks 114–34 leaf-cutter ants 9, 42–3
alternative stable states 132–4 in decomposition 47
direct effects 114, 116 and dung beetles 44
ecosystem productivity in 135–6 and nitrogen-fixation 43
indirect effects 116 leaf dry matter content 82
 Index • 295

leaf-height-seed (LHS) model 134–5 affecting nitrogen forms in soil 20, 23

leaf properties, alien vs native species 183–4 and climate change 54, 100–1
legumes and earthworms 41–2 competition for nutrients 19
LHS (leaf-height-seed) model 134–5 and element availability 85
lignins 6, 66 extreme weather, effects of 55–6
litter decomposition and heavily-grazed grassland 154
alien vs native species 184–5 herbivory, effects of 126, 154
and climate change 53–5, 102, 106 invasive 190–1
decomposer–plant relationship 88 microbial grazing 8, 24–5
selection of decomposer by plant 64, 89, 90, and decomposition 48
203, 212–13 multiple plant species, effects of 72
and foliage palatability 136 nitrogen immobilization 23
and litter quality 76, 77, 79 in nitrogen partitioning 23
and plant traits 75–6 nitrogen retention 19
selective feeding effects 123 plant growth, effects on 18–22, 23
soil fauna removal 179 predation, effects of 24–5
trophic cascades, effects of 27 removal experiments 178
in vegetation succession 92 seasonal dynamics 19–20, 21
litter loss of understanding 59–60
across growth forms 105 in vegetation succession 92
biotic/abiotic drivers 104 ‘microbial loop’ 24
and climate change 102 midges 151
macro-detritivore diversity, effects of 48–9 Millennium Ecosystem Assessment 14
and temperature 105 mites
litter-mixture studies 74, 168–9 and herbivory 128, 129
mass ratio hypothesis 82 in soil food web 26
litter quality in trophic cascades 27
carbon dioxide, effects of 11 Molinia caerulea 66, 88, 98
and climate change 102 monocultures and soil organism biomass 64, 72, 74
in coexisting species 78 moose
decomposition, effects on 8, 77, 79 nutrient transfer
in ecosystem retrogression 96–7 as carcasses 146
and herbivory 136 freshwater to land 149
predators on, effects of 139 and predators 139, 181
interspecific differences 6, 64, 66–7, 77 selective feeding effects 123, 124
landform variation, effects of 77, 78 mosses see bryophytes
and nitrogen enrichment 108 moths 194, 195
and plant traits 75, 76, 77–9, 136 mull and mor theory 62
and resource acquisition 7 multiple species communities 216
selective feeding effects 123 multiple species effects see plant diversity
litter stoichiometry 84–5 mushrooms
litter transformers 40 and invasion 191
Lolium perenne 41, 73 phenology and climate change 54–5
Lupinus spp. 33, 86 mutualistic relationships
Lymantria dispar 195 plant–decomposer 87–8
plant–soil
mathematical models 4–5 and plant communities 90
Metrosideros polymorpha 68 soil biota–host plants 16, 86
mice, invasive 193–4 as succession drivers 97
microarthropods and vegetation dynamics 39 mycorrhizal fungi 52
microbes in biodiversity 37–8
aboveground predators, effects of 140 carbon exchange 50, 51–2
296 • Index

mycorrhizal fungi (cont.) New Zealand flatworm 193, 194

and climate change 100 New Zealand (Franz Josef glacier)
defoliation, effects of 127 chronosequence 93, 95, 96
herbivory, effects of 127 New Zealand (Waitutu) chronosequence 93, 94,
mutualistic relationships 86–7, 212 95, 96
nitrogen transfer 33–4 nitrification 23
and plant community dynamics 9, 35–8, 59 nitrogen
in plant productivity 37 C:N ratio 28, 29, 30
and plant traits 76, 77 competition for 19–20
tree roots, effects of 67 and dung beetles 44
in vegetation succession 91–2, 97 global emissions 11
Myrica spp. 6, 32, 185 immobilization 101
and symbiotic bacteria 190 in litter 84
microbial pool 19, 23
Narthecium ossifragum 66 N:P ratios
NEE see net ecosystem exchange in ecosystem retrogression 93–4
negative feedbacks 4 in litter 78
to global warming 102 Redfield ratio 95
plant palatability in 7 in vegetation 84
plant–herbivore 9–10 partitioning
plant–pathogen 38 by chemical form 20, 22–3
plant–soil 86 seasonal 19–20
rare native plants 187, 188 retention 30–1
vegetation succession 97–8, 217 seasonal dynamics 21
nematodes soil fungal:bacterial ratio 28, 29, 30–1
and climate change 54, 55 transfer of
in ecosystem retrogression 96 freshwater to land 149–51
invasion by 191 legumes to grasses 33–4
negative feedbacks with plants 87 uptake 18–19, 20, 22
and net primary production 64, 65 see also soil nitrogen; total soluble nitrogen
in nitrogen uptake 8 pool
numbers in soil 15 nitrogen availability 59
and plant productivity 25 and climate change 101
root-feeding, species identity of 170 plant species effects 5
in soil food web 26 and plant species self-replacement 108
and vegetation dynamics 39 in vegetation succession 92
and wireworms 40 nitrogen cycling 59
net ecosystem exchange (NEE) herbivore-induced acceleration 116–20
grazing, effects of 155–7 nitrogen deposition 11, 12
geese 157 belowground effects via vegetation 107–10
reindeer 157 experiments 109–10
sheep 156–7, 158 nitrogen enrichment
inter-annual variation 157 and climate 107
net primary production (NPP) and climate change 12
and biodiversity 167, 171 interaction with soil subsystem 110
grazing, effects of 126–7 and litter quality 108
optimization by grazers 116 by seabirds 148
and plant traits 81 soil organisms, effects on 11–12, 58
and shrub expansion 205 nitrogen fixation
and soil fertility 223 and climate 33
species effects 64, 65 in ecosystem retrogression 93–4
temporal variability 71–2, 217 and vegetation succession 33–4
 Index • 297

nitrogen fixers palatability see foliage palatability

ecosystem, effects on 5–6 pathogens
free-living/associative 34–5 aboveground invasive 195–201
and plant productivity 32–3 soil-borne
symbiotic 33 antagonistic relationships 87
nitrogen-fixing bacteria promotion by target plants 87, 220
cyanobacteria 9, 34, 35 and vegetation dynamics 38–9
in species removal experiments 176 and vegetation succession 39
diversity, importance of 170–1 peat/peatlands
ecosystem, effects on 9 carbon dioxide/temperature, effects of 57
and invasion 189–90 drought, effects of 56
and leaf-cutter ants 43 penguins 148
in vegetation succession 91 permafrost 56, 60–1
nitrogen-fixing shrubs, alien vs native 185 phenolic compounds
nitrogen-limited ecosystems degradation 21, 56
amino acid uptake 18–19 interspecific differences 6, 66, 67
seasonal dynamics 20, 21 phosphorus
nitrogen mineralization 18, 30 in litter 84
earthworms in 47 N:P ratios
and plant species 62 in ecosystem retrogression 93–4
Rhinanthus minor, effects of 29, 31 in litter 78
selective feeding effects 124 Redfield ratio 95
non-nutritional links 8 in vegetation 84
Nostoc spp. 35 partitioning 22
Nothofagus sp. 88, 89, 196, 198 redistribution by grazers 143–4
novel weapons hypothesis 189 and selective browsing 124
nutrient availability phosphorus availability 19
and ants 42–3 long-term loss 93
in ecosystem retrogression 93, 96 phosphorus mineralization 19, 47
liberation from microbial biomass 23–4 Phytophthora spp. 191
microbial predation, effects of 23, 24–5 Picea spp. 33, 44
plant growth, effects on 17–23 spatial distribution 71
plant–microbe competition 19–20 temporal variability 72
soil trophic interactions, effects of 23–6 pigs 128, 196
and termites 42 Pinus spp. 33, 68, 98
top-down control 24 invasive 185, 186, 189
nutrient cycling plants
bacterial/fungal-based energy channels 28–32, own-litter decomposition 64, 89, 90, 203, 213
60 pathogen promotion 87, 220
C:N ratio 28, 29, 30 range changes 201–2, 203
herbivore-induced change 116, 125, 126 shrub expansion 102, 203–4, 205
soil fauna, effects of 25 plant communities
nutrient enrichment model 24, 32 belowground effects 62–112
nutrient-limited ecosystems, competition in decomposer selection 88, 89
19 and dung beetles 44–5
nutrient mineralization dynamics
bacterial/fungal energy channels 28–30 arbuscular mycorrhizal fungi 9, 36, 37
and predator-induced trophic cascades 27 and ecosystem engineers 40–5
nutrient retention 30–1 ecosystem, effects on 7
grazing and warming, effects of 160
Ophiostona spp. 195 and root-associated biota 32–8
overgrazing 128, 132 soil community, effects on 62–112, 213–14
298 • Index

plant communities (cont.) in climate change 105–6

multiple species effects 72–4, 82, 84 ferns/bryophytes 79, 80
plant species variation 63–7 within-species variability 79
spatial/temporal variability 70–2 and species 75–9
within-species variation 68–70 and species loss 176
within-species genetic variability 68 trait dominance/dissimilarity 75–9
see also vegetation dynamics; vegetation vs plant species 75–80
succession Plantago spp. 73, 139
plant diversity (multiple species effects) Pleurozium schreberi 9, 34–5
plant traits 82, 84 Poa pratensis 121
soil community, effects on 72–4 polyphenols see phenolic compounds
plant growth Pontoscolex corethurus 192
nutrient availability, effects of 17–23 Populus spp.
soil trophic interactions, effects of 23–6 secondary metabolite accumulation 126
plant palatability 7 spatial distribution 71
plant polysynthate, ‘age’ of 50, 51, 60 within-species variability 68, 69
plant species positive feedbacks 4
decomposition, effects on 8, 168 decomposition–climate change 11
ecosystem, effects on 5–6, 62 plant palatability in 7
stability 171 plant production–nitrogen cycling 108–9
soil processes, effects on 167, 168 plant–decomposer 90, 213
spatial segregation 71 plant–herbivore 10
as soil type determinants 5 plant–soil 86
in vegetation succession/disturbance 92 invasive plants 187, 188
vs plant traits 75–80 prairie dogs 122
plant symbionts see mycorrhizal fungi; nitrogen precipitation patterns 101–2
fixers predation of microbes 24–5
plant trait databases 6 predators
plant traits and belowground subsystem 139
acquisitive strategy and litter quality 7 climate change, effects of 161
alien vs native species 183–5 decomposer food webs, effects on 141
analysis 6 ecosystem, effects on 7
and carbon pools 106, 107 invasive species 199
in coexisting species 76–7, 216, 219 herbivory, effects on 7, 137, 138–9
community-weighted values 81 invertebrate 139–40
consumers, effects on 215–16 variability of effects 141
and decomposition 75–6 invasive species 196, 199
defoliation, responses to 136–7 losses, effects of 181
as ecological drivers 214–16, 219 in soil food web 26–7
ecosystem stoichiometry 84–5 of soil organisms, invasive 193
effect on plant–herbivore interactions Prinlgeophags marioni 194
6–7 pronghorn antelope
and fertility/herbivory levels 118 exclusion experiments 115
grazing, favoured by 135 grazing, effects of 119
herbivore impacts, regulating 134–7 and nitrogen cycling 144
belowground processes in 136–7 protists 25
models 134–5 protozoa 191
intraspecific variation 215 Prunus serotina 87, 188, 220
and litter quality 75
multiple species effects 82, 84 Queensland (Coolcoola) chronosequence 93, 94,
non-foliar 215 95
soil community, effects on 75–85 Quercus spp. 195
 Index • 299

rabbits 119, 123, 143 seasonality 20

range changes/expansion 12, 201–7, 225–6 soil organisms, effects on 10, 24
causes 207 root herbivory
herbivores negative feedbacks with plants 87
insects 204, 206–7 and vegetation dynamics 39–40
mammals 207 root productivity and grazing 122
northward/upward shift 202
plants 201–2, 203 salamanders 179
shrub expansion 102, 203–4, 205 Salix glauca 160
range-succession model 134 salmon, nutrient transfer by 149–51
rats 199, 200 Scottnema lindsayae 54, 55
red deer 115, 124, 125, 126 seabirds
Redfield ratio 95 and invasive species 199, 200
reindeer nutrient transfer by 148–9, 151
disturbance by 128 plant limitation by 149
exclusion experiments 115 secondary metabolite accumulation 126
grazing, effects of 157 sheep
NEE, effects on 157 exclusion experiments 115
and vegetation states 132, 133–4 grazing, effects of 118, 156–7, 158
wastes, effects of 119, 120 shrub expansion
removal experiments see species removal and aboveground NPP 205
experiments and climate change 203–4
resource acquisition and soil carbon 102
adaptation for 6, 221 snow cover reduction 55, 56–7
and litter quality 7 soil biota
nutrient transfer by seabirds 148, 163 and host plants 16
vs conservation 75 loss of microbial subsets 178
resource conservation, adaptation for 6 range changes 203
resource movement by consumers 131, removal experiments 176, 178
141–51 variation, global 222–3
across land 141–7 soil carbon
aquatic to terrestrial ecosystems 147–51 C:N ratio 85
resource pulses soil fungal:bacterial ratio 28, 29, 30
from carcass deposition 144–5, 147, 217 dynamics
after foliar herbivory 119, 121 and climate change 13
seasonality 20, 21 seasonal 21
spatial variability 163 herbivores, effects of 152–4
temporal variability 72 historical perspective 5
respiration see soil respiration loss, factors affecting 57
Rhinanthus minor 29, 31 and plant traits 106, 107
Rhizobium spp. 32, 189 see also soil organic carbon pool
root-associated biota 9 soil fauna
and invasive species 12 body size and trophic cascades 27–8
and plant community dynamics 32–8 and decomposition rates 50, 51
and plant species 62–3 and element availability 85
root biomass grazing activities, effects of 25, 52, 60
grazing, response to 154, 155 invasive plants, effects of 185–7
and soil carbon stores 154, 155 invertebrates, invasion by 191–2
root exudates macrofauna
grazing, effects of 121 in decomposition 47
interspecific differences 67 diversity and respiration/
plant communities, effects on 62 decomposition 49–50
300 • Index

soil fauna (cont.) plant productivity, effects of 62

as ecosystem engineers 45 plants, effects of
in ecosystem retrogression 96 spatial patterning 70–1
invasion by 192 temporal variability 71–2
invasive herbivores, effects of 196, 197 tree roots 67
removal experiments 178–9 soil community, effects on 213
traits 216 taxonomic problems 15, 214
in vegetation succession 98 new techniques 214
soil fertility and climate change 223–4 soil respiration
soil food web 16 autotrophic/heterotrophic 50, 51–2
bottom-up vs top-down control 63–4 and climate change 52–4, 101
in ecosystem retrogression 96 drivers 50
grassland 24, 26 multiple plant species, effects of 73
Hunt’s soil food web model 24, 26 and polysynthate ‘age’ 50, 51, 60
invasion, effects of 199, 200 soil macrofauna 45, 46–7, 48
invasive plants 185 diversity 49–50
plant entry into 46 tree roots, effects of 67
positive feedbacks with plants 87–8 soil science, historical perspective of 8
trophic cascades 26–8 soil structure and macrofauna 45
in vegetation succession 92 soil temperature and grazing 122–3
soil food web model 5 Solidago altissima 68, 69
soil fungal:bacterial ratio 30 space-for-time substitution 3
C:N ratio 28, 29, 30 spatial patterning 70–1
nutrient retention 30–1 species diversity see biodiversity
Rhinanthus minor, effects of 29, 31 species effects as ecosystem drivers 5–8
soil nitrogen species losses/gains
competition for 19 consequences 165–210
composition 18 as consequences of global change 201–7
soil organic carbon pool 45, 46 and decomposition 48
in climate change 106 ecological effects 166, 181–3
soil organisms ecosystem, effects on 13, 165–210, 225–6
carbon cycle, effects on 52–7 gains through invasion 183–201
carbon dioxide, effects on 11 aboveground consumers 195–201
and climate change 52–7 belowground invaders 190–5
extreme weather events 55–6, 224 human-induced factors 165
nitrogen enrichment 110 by plants 183–90
in decomposition/respiration 46–7 invasive vs native species 183–7
ecosystem carbon exchange 46–52 plant–soil feedbacks 187–90
food webs 16 losses through extinction 166–83
and global change 45–59 aboveground–belowground
land use changes 57–8 perspective 166–72
nitrogen enrichment 58 experimental approaches 180
historical perspective 15 human-induced factors 165
multiple plant species, effects of 72 non-random 173
nitrogen enrichment, effects of 11–12 in real ecosystems 179–83
numbers/amounts 15 removal experiments 172–9
plant communities, effects of 62–112 species traits 180–1
multiple species effects 72–4 range changes 201–2
plant species variation 63–7 through human activity 179–80, 181
plant traits 75–85 consequences of 201–7
spatial/temporal variability 70–2 species removal experiments 81, 83, 172–9
within-species variation 68–70 ericaceous shrub removal 175, 176, 177
 Index • 301

grassland plant group removal 174–5 and soil food web 26–8
removal approach 173–4 environmental factors 27–8
soil biota 176, 178 trophic dynamic theory 6–7
soil macrofauna 178–9 historical perspective 3
vertebrate herbivores 179 trophic interactions 8
species replacement in vegetation succession 97 in soil 23–6
species richness see biodiversity Tsuga spp. 195
species traits and extinction 180–1 tundra ecosystems see arctic ecosystems
spiders 27, 179
state factor concept 3 Ulmus spp. 195
succession see vegetation succession
Sweden (Arjeplog) chronosequence 93, 95 Vaccinium myrtillus 67, 160, 176, 177
symbiosis 38 Vaccinium vitis-idaea 176, 177
vegetation collapse 132, 133
temperature vegetation composition
biological activity, effects on 46, 52–5, 56, and climate change 102, 103, 160–1
60–1 and herbivory 125–6, 160–1
and faunal effects on decomposition 50 vegetation dynamics
see also climate change and ants 42–4
termites and dung beetles 44–5
in decomposition 47 and earthworms 41–2
as ecosystem engineers 42 and root herbivory 39–40
mounds/nests 41 and soil pathogens 38–9
spatial variability, drivers of 220 vegetation succession
total soluble nitrogen pool 18 and ants 44
traits build-up phase 91–3
and extinction 180–1 decline/retrogressive phase 91, 93–7, 218–19
fungi 216 and disturbance 90–9
soil fauna 216 and ecosystem retrogression 93–7
see also plant traits and mycorrhizal fungi 37
‘tree islands’ 71, 219 and nitrogen fixation 33–4
trees and plant–soil feedbacks 97–9
harvesting, effects of 173 primary 91
invasive pathogens 195 removal experiments 82, 83
litter decomposition rates 88 secondary 91
multiple species effects 72, 73 and soil pathogens 39
N:P ratios in functional groups 84 species replacement 97
plant traits in coexisting species 76
root exudates 67 Waitutu (New Zealand) chronosequence 93, 94,
Trifolium repens 41 95, 96
trophic cascades 7 water infiltration 45
aboveground weather events, extreme
effects on belowground properties consequences 224–5
137–41 and soil organisms 55–6
mechanism 138 wireworms 39, 40
ants, triggered by 44 wolves 181
aphid-predators, triggered by 139–40 and herbivore carcasses 146
decomposition, effects on 48 reversing cervid herbivory effects 138–9