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Ecological indicators and surrogates are used widely by resource managers to monitor and

Indicators and Surrogates of Biodiversity and Environmental Change

understand complex biota and ecosystem processes. Their potential to guide complex resource
management has meant they have been proposed for use in all ecosystems worldwide. Despite
extensive research into indicators and surrogates, there remains much controversy about their
use, in addition to major issues and knowledge gaps associated with their identification, testing
and application.

Indicators and Surrogates of Biodiversity and Environmental Change provides insights

into the use of indicators and surrogates in natural resource management and conservation –
where to use them, where not to use them, and how to use them. Using an ecological approach,
the chapters explore the development, application and efficacy of indicators and surrogates in
Indicators and Surrogates
terrestrial, aquatic, marine and atmospheric environments. The authors identify current gaps
in knowledge and articulate the future directions for research needed to close those gaps. of Biodiversity and
Environmental Change
This book is written by the world’s leading thinkers in the area of indicators and surrogates.
It is the first major synthesis of learnings about indicators and surrogates and will be a critical
resource for the vast number of people developing and applying them in ecosystems around
the world.

About the editors

David Lindenmayer is a Research Professor at the Fenner School of Environment and
Society at The Australian National University. He leads a range of large-scale, long-term
field-based programs examining the impacts of land use practices such as forestry, plantation
management and agricultural development on biodiversity.

Philip Barton is a Research Fellow at the Fenner School of Environment and Society at The
Australian National University. He is a community ecologist with a particular interest in insects.
Philip is currently working on theoretical and empirical assessments of biodiversity surrogates.

Jennifer Pierson is a Research Fellow at the Fenner School of Environment and Society

David Lindenmayer, Philip Barton and Jennifer Pierson

at The Australian National University. She is a population ecologist interested in the
interacting contributions of behaviour, demography and genetics to population dynamics.

Editors: David Lindenmayer, Philip Barton and Jennifer Pierson

Indicators and Surrogates
of Biodiversity and
Environmental Change
Editors: David Lindenmayer, Philip Barton and Jennifer Pierson
 This page intentionally left blank

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Indicators and Surrogates
of Biodiversity and
Environmental Change

Editors: David Lindenmayer, Philip Barton and Jennifer Pierson

© Professor David Lindenmayer, Dr Philip Barton Published exclusively throughout the world
and Dr Jennifer Pierson 2015 (excluding Australia and New Zealand) by CRC
Press, with ISBN 978-1-4987-4870-4
All rights reserved. Except under the conditions
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Lindenmayer, Philip Barton and Index by Bruce Gillespie
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Includes bibliographical references and index. autonomously from the research activities of the
Environmental indicators. Commonwealth Scientific and Industrial Research
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Environmental management. publication are those of the author(s) and do not
Biodiversity conservation. necessarily represent those of, and should not be
attributed to, the publisher or CSIRO. The copyright
Lindenmayer, David, editor.
owner shall not be liable for technical or other errors
Barton, Philip, editor.
or omissions contained herein. The reader/user
Pierson, Jennifer, editor.
accepts all risks and responsibility for losses,
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Published exclusively in Australia and New Zealand directly or indirectly from using this information.
by Original print edition:
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Contents

Acknowledgements vii
Author biographies ix

1 Introduction – disciplinary and multi-disciplinary perspectives on

ecological indicators and surrogates 1
David Lindenmayer, Jennifer Pierson and Philip Barton

2 Surrogates for the distribution and trajectory of biodiversity 5

Martin Westgate

3 Biodiversity surrogates 15
David Lindenmayer, Philip Barton, Martin Westgate, Peter Lane and Jennifer Pierson

4 Conservation by proxy: thoughts 5 years on 25

Tim Caro

5 Avian surrogates in terrestrial ecosystems: theory and practice 33

Kathy Martin, José Tomás Ibarra and Mark Drever

6 Using decision theory to select indicators for managing threats

to biodiversity 45
Ayesha Tulloch

7 Invertebrate indicators and ecosystem restoration 59

Philip Barton and Melinda Moir

8 Mosses as passive and active indicator surrogates for

investigations of atmospheric pollution and quality 69
Hanna Salo

9 Lichens as ecological indicators to track atmospheric changes:

future challenges 77
Cristina Branquinho, Paula Matos and Pedro Pinho

v
vi Indicators and Surrogates of Biodiversity and Environmental Change

10 Approaches, potential and pitfalls of applying bioindicators in

freshwater ecosystems 91
Jani Heino

11 Searching for the holy grail of wetland integrity: are surrogates

still relevant in conservation planning? 101
Hamish Greig and Aram Calhoun

12 Surrogates for coral reef ecosystem health and evaluating

management success 113
Maria Beger

13 Abiotic surrogates in support of marine biodiversity

conservation 125
Camille Mellin

14 Building indicators for coupled marine socio-ecological systems 137

Catherine Longo and Benjamin Halpern

15 The application of genetic indicators in wild populations:

potential and pitfalls for genetic monitoring 149
Jennifer Pierson, Gordon Luikart and Michael Schwartz

16 Use of surrogates in medicine: ideas that may be useful for

ecology 161
Peter Lane and Philip Barton

17 Application of surrogates and indicators to monitoring natural

resources 169
John Gross and Barry Noon

18 Indicators and surrogates in environmental management 179

William H. McDowell

19 A diversity of approaches to ecological surrogates and key

knowledge gaps 189
David Lindenmayer, Jennifer Pierson, Philip Barton, Peter Lane, Ayesha Tulloch and
Martin Westgate

Index 195
Acknowledgements

We thank Tabitha Boyer and Claire Shepherd for many aspects of book production as well
as organising the workshop that instigated the writing of all of the chapters that feature in
this book.
We thank Mac Hunter for contributing to the workshop and assisting with the synthesis
of ideas.
We most gratefully acknowledge the support of John Manger from CSIRO Publishing
in encouraging this book to be written.
A number of the chapters in this volume feature scientists from the Fenner School of
Environment and Society at The Australian National University. These scholars are sup-
ported through an Australian Research Council grant (to DBL). We are indebted to that
organisation for its support.
Finally, the editors thank all chapter authors for the rapid responses to constant badg-
ering to deliver timely but high quality written material.

David Lindenmayer
Jennifer Pierson
Philip Barton
(The Editors)
December 2014

vii
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Author biographies

Philip Barton is a Research Fellow in the Fenner School of Environment and Society,
ANU. He is a community ecologist with a particular interest in insects. Philip is currently
working on theoretical and empirical assessments of biodiversity surrogates.

Maria Beger is a Research Fellow in the Centre for Biodiversity and Conservation Science
at the University of Queensland, Australia. Her research employs interdisciplinary empiri-
cal and modelling approaches to aid decisions about managing marine ecosystems. She
works at better incorporating bio-physical and ecological processes into decision sci-
ence that challenge effective management in the face of climate change, an increasing
human footprint and transforming ecosystems.

Cristina Branquinho is an Associate Researcher at the Universidade de Lisboa. She is an

ecologist with particular interest in lichens and plants. Cristina is currently interested in
ecological indicators of nitrogen pollution and of climate change based on functional
diversity.

Aram Calhoun is a wetland ecologist in the Department of Wildlife, Fisheries, and Con-
servation Biology at the University of Maine, USA. Her research focuses on forested wet-
lands and vernal pool ecosystems. She is particularly interested in collaborative approaches
to conserving natural resources on private lands. Dr Calhoun is active in working at all
levels of government (local, state, and federal) on wetland policy and conservation issues.

Tim Caro is a Professor of Wildlife Biology at the University of California at Davis whose
research focuses on behavioural ecology and conservation biology, particularly strategies
to conserve wildlife in tropical ecosystems. He runs a long term field site in Katavi National
Park western Tanzania. He recently published a book entitled Conservation by Proxy: Indi-
cator, Umbrella, Keystone, Flagship, and other Surrogate Species in which he tried to bring
order to this area of conservation. His current conservation work in Africa includes iden-
tifying wildlife corridors and understanding threats to protected areas.

Mark Drever is a population ecologist with the Canadian Wildlife Service of Environment
Canada and Adjunct Professor with the University of British Columbia. He conducts
research on the conservation of migratory birds, focusing on shorebirds and waterbirds.

Hamish Greig is a freshwater ecologist in the School of Biology and Ecology at the Univer-
sity of Maine, USA. His research focusses on communities of invertebrates and fish in
stream, river, lake and wetland ecosystems. He is particularly interested in the impacts of

ix
x Indicators and Surrogates of Biodiversity and Environmental Change

disturbance on freshwater communities, and is currently working on understanding and

measuring the impacts of climate change and catchment modification on freshwaters.

John Gross is an ecologist with the US National Park Service. He was with the NPS Inven-
tory & Monitoring Program during the development and implementation of natural
resource monitoring across nearly 300 park units. John’s background is in ecological mod-
elling and his current focus is on climate change adaptation in protected areas.

Ben Halpern is a Professor in the Bren School of Environmental Science & Management at
UC Santa Barbara and Chair in Marine Conservation at Imperial College London. He
focuses his research at the interface between marine ecology and conservation planning.
He has led and participated in several key synthetic research projects that have advanced
our understanding of the state of the world’s oceans and the potential for marine reserves
to improve ocean condition. In particular he has led the development and mapping of
cumulative impact assessments at global and regional scales in marine and freshwater
systems and has been the lead scientist for the Ocean Health Index project.

Jani Heino is a Research Professor at the Finnish Environment Institute. He is an ecologist

interested in biodiversity, mechanisms underlying its origins, maintenance and variation,
and its conservation and management in the face of environmental changes. His current
studies focus mainly on streams, rivers, ponds and lakes.

José Tomás Ibarra is a Postdoctoral Researcher in the Department of Forest and Conser-
vation Sciences at the University of British Columbia, Canada. He is a community ecolo-
gist with broad interests in natural history and the influence of multiple factors (e.g.
habitat, biotic interactions and land-use changes) in shaping the current state of taxonomic
and functional animal biodiversity. During his PhD, José Tomás studied the ecology of
poorly known owls in Andean temperate forests, and validated forest-specialist owls as
surrogates for both taxonomic and functional biodiversity in this globally threatened
eco-region.

Peter Lane is a Statistical Consultant in the Fenner School of Environment and Society,
ANU. He is a statistician, working in David Lindenmayer's team on surrogacy. Previously,
he worked for 13 years as a research and consultant statistician in the pharmaceutical
industry (GlaxoSmithKline), and for 25 years in agricultural research at Rothamsted in the
UK.

David Lindenmayer is a Research Professor at the Fenner School of Environment and

Society, ANU. He leads a range of large-scale, long-term field-based programs examining
the impacts of land-use practices such as forestry, plantation management and agricultural
development on biodiversity.

Catherine Longo is a project scientist at the National Center for Ecological Analysis and
Synthesis (NCEAS, USA). Her expertise is in indicators for coupled socio-ecological
marine systems (www.oceanhealthindex.org), and her fields of interest are fisheries,
biodiversity, metabolic theory, data-poor assessments and evaluating uncertainty.

Gordon Luikart is a professor of Conservation Genetics at the Flathead Lake Biological

Station and University of Montana. He has conducted research on the genetics and conser-
 Author biographies xi

vation of fish and wildlife for over 15 years in the USA, France, and Portugal. His primary
focus has been on the development and application of molecular genetic and computa-
tional tools for assessing the genetic basis of fitness, and monitoring effective population
size and landscape genetic connectivity.

Kathy Martin is a Professor in the Department of Forest and Conservation Sciences

at the University of British Columbia and a Senior Research Scientist with Environment
Canada, Vancouver Canada. She is a population and community ecologist with a particu-
lar interest in responses of birds to environmental and habitat disturbance in forest and
alpine ecosystems. Kathy is currently working on theoretical and empirical assessments of
biodiversity surrogates and indicators for cavity-nesting vertebrates experiencing insect
outbreaks and forest harvesting, as well as the responses of mountain birds to climate
change impacts in the Americas.

Paula Matos is a PhD Candidate at the Universidade de Lisboa and the Universidade de
Aveiro, Portugal. She is an ecologist with particular interest in lichens. Paula is currently
interested in ecological indicators of climate change and air pollution based on lichen
functional diversity.

William H. McDowell is a Professor of Environmental Science in the Department of Nat-

ural Resources and the Environment, University of New Hampshire, USA. He is an eco-
system ecologist and biogeochemist with a particular interest in understanding the role of
dissolved organic matter in aquatic and terrestrial ecosystems. He is currently working on
several long-term projects to understand land–water connections in forested watersheds.
He has recently begun to deploy real-time water-quality sensors in order to understand
drivers of water quality at time scales from minutes to decades.

Camille Mellin is an ARC Discovery Early Career Research Award fellow at the Austral-
ian Institute of Marine Science (AIMS). Camille is a quantitative ecologist with a back-
ground in marine and coral reef ecology. She is currently working on the predictive
modelling of Acanthaster planci (crown-of-thorns starfish) outbreaks, coral reef resilience
to disturbance and biodiversity patterns.

Melinda Moir is an Assistant Professor at the School of Plant Biology at the University of
Western Australia. She is a research entomologist with projects on conservation biology,
extinction risk, refugia in climate change, traits across trophic groups in ecological resto-
ration, and invasion ecology.

Barry Noon is a Professor in the Department of Fish, Wildlife, and Conservation Biology
at the Colorado State University. He has conducted research on the effects of land
management practices on wildlife populations in the USA and internationally for more
than 40 years. His primary research focus has been on the population dynamics and con-
servation of imperilled species in terrestrial ecosystems.

Jenny Pierson is a Research Fellow in the Fenner School of Environment and Society,
ANU. She is a population ecologist interested in the interacting contributions of behav-
iour, demography and genetics to population dynamics. She is currently working on
empirical assessments of biodiversity surrogates, with a focus on genetic indicators and
habitat-based surrogates.
xii Indicators and Surrogates of Biodiversity and Environmental Change

Pedro Pinho is a Post-doctoral Fellow at the Universidade de Lisboa working on the use of
vegetation functional groups and spatial patterns to assess the effect of environmental
changes, with both natural and human origin: desertification and land degradation,
climate change, eutrophication and land-use/cover.

Hanna Salo is currently a PhD candidate in the Department of Geography and Geology,
University of Turku, Finland. She is a geographer focusing on environmental research,
with the main emphasis on air quality issues. At present, Hanna is working on magnetic
biomonitoring of atmospheric pollution and especially heavy metals.

Michael Schwartz is the Director of the National Genomics Center for Wildlife and Fish
Conservation located in Missoula Montana. He is a Presidential Early Career Award in
Science and Engineering recipient and an adjunct faculty member of the University of
Montana’s College of Forestry and Conservation. Dr Schwartz’s research team focuses on
the fields of population, conservation and landscape genetics. He seeks to provide practical
answers to natural resource problems, combining field and laboratory work.

Ayesha Tulloch is a Research Fellow at the Fenner School of Environment and Society,
ANU. She is interested in solving problems of resource allocation to monitoring and man-
agement of biodiversity. She is currently working on applications of surrogates in adaptive
management of threatened birds, and exploring how variability in species associations can
affect decisions such as optimal indicator selection that rely on surrogacy data for inform-
ing monitoring choices.

Martin Westgate is a Research Fellow in the Fenner School of Environment and Society,
ANU. He is an ecologist interested in how ecosystems respond to natural and human-
induced change, and is currently working on biodiversity surrogates and meta-analyses of
cross-taxon congruence.
1

Introduction – disciplinary and multi-disciplinary

perspectives on ecological indicators and
surrogates

David Lindenmayer, Jennifer Pierson and Philip Barton

Introduction
The term surrogate can be broadly defined as a proxy for something else. The scientific
study of ecological surrogacy, and its application to biodiversity and resource manage-
ment, is widespread – more than 5000 scientific articles have been published on the topic
(Westgate et al. 2014). The reason for this vast literature is the natural environment is so
complex that it is neither logistically practical nor financially possible to directly measure
and monitor all components of the environment in all locations and at all times. Surro-
gates or proxies are therefore needed to represent other attributes of the environment that
are not able to be directly measured (Caro 2010; Collen and Nicholson 2014). Indeed, the
application of ecological surrogates lies at the heart of many key areas of environmental
science, ranging from the selection and monitoring of reserves, monitoring of pollutants
in the atmosphere or drinking water, the effectiveness of vegetation restoration, and esti-
mates of the number of the total number of plant and animal species in a given location.
The primary focus of this edited volume is on ecological surrogates – although, as we
discuss below, our book also includes a chapter on the use of surrogates in medicine and
insights on surrogacy from statistical science. However, before we outline some of the con-
tent of this book, the reason why it was written and the structure used to guide each chap-
ter, it is important to first define at the outset what we mean by the term ‘surrogacy’, and
other terms that fall within its broader remit (in particular the term ‘indicator’). We also
highlight the important distinction between surrogacy and direct measurement (sensu
Lindenmayer and Likens 2011).
For the purposes of this book, we deem the term surrogate to mean a proxy for some
other entity. The primary focus of this book is on ecological surrogates; that is, the use of
proxies in the environment, ecology and conservation. Direct measurement in the context
of this book means measuring a given entity without implying that it is a proxy for some
other entity (Lindenmayer and Likens 2011). For example, the concentration of E. coli in an
aquatic ecosystem might be measured simply to determine how much of this microorgan-
ism occurs in a given water body. Similarly, the concentration of carbon dioxide in the

1
2 Indicators and Surrogates of Biodiversity and Environmental Change

atmosphere (e.g. the Keeling curve) may simply be a direct measurement of how much of it
now occurs in the air above a given area. These direct measurements of E. coli and carbon
dioxide do not have to imply anything about the condition of the airshed or of the water.
However, if the amount of E. coli is considered to a proxy for the quality of water fit for
human consumption or the concentration of carbon dioxide as a proxy for future increases
in temperature, then they become ecological surrogates – that is, a proxy for some other
entity (water quality or future temperature).
Why is there a need to define these terms? The reason is that many terms in the rele-
vant literature (including the term surrogate itself) have been used in quite different ways
and to mean quite different things. This is evident even in this book. Hence, we have asked
the author/s of each chapter to specifically define key terms within the text to ensure that
readers understand the particular usage.

The aim of this book

There have been many detailed reviews of ecological surrogacy, and the narrower field of
species-based indicators, in recent years (e.g. McGeoch 1998; Niemi et al. 1997; Rodrigues
and Brooks 2007; Caro 2010). The purpose of this book was not to cover the same ground
as these previous reviews. Rather, it was to highlight the diverse ways that surrogacy is
studied and applied in the broader environmental sciences, including terrestrial, marine,
aquatic, atmospheric and policy realms. Our aim was then to draw together some of the
key learnings from these different disciplines and compare and contrast the different ways
the study and application of surrogates have evolved within them. In addition, we sought
to explore the overlap and divergences between disciplines in the use of ecological surro-
gates with an explicit aim of trying to uncover ways to improve the application of surro-
gates in the future.

The structure of this book and the chapters

As part of compiling this book, we asked chapter authors not to re-hash what they have
written previously, but rather to expound their personal views on their important area of
expertise. In particular, authors we asked to arrange their chapters around 10 points that
cover things they have learnt or are known, and remaining challenges or unknowns in
their field. The focus was largely on practical (realistic) applications of indicators and sur-
rogates in environmental management and/or conservation management. Each chapter
covers discipline-specific areas, and many use terminology developed and used by
researchers in that field. Acronyms have been avoided where possible, and definitions pro-
vided where necessary.
Each chapter in this book has been kept deliberately short and to the point. This was
done for good reason – the information ‘super-glut’ of this era means that there is an over-
load of information that few people have time to touch on, evenly briefly. Our aim was
therefore to request chapter authors to produce short pithy chapters that were readily
accessible and with the key points summarised in a way that could be quickly compre-
hended. The challenge to all authors was to summarise their ideas in a few thousand words
– and shorter if possible. To this end, each chapter is structured in a similar way. That is:
• A box with the 10 dot points – one for each key issue that they considered.
• A few short introductory paragraphs with limited background on their topic.
 1: Introduction 3

• Approximately five things that have been learnt or are known, and five remaining
challenges or unknowns in their field, with one or two paragraphs on each of the 10
key issues.
• A paragraph on each issue laying out why it is essential that it must be tackled.
• A small set of references directing readers to additional literature that further
explores the topic.
This book is broken into six main themes. Theme 1 contains four chapters and is a gen-
eral overview of ecological indicators and surrogates, including global perspectives on
their use. Three chapters comprise theme 2, which is focused on ecological indicators and
surrogates in the terrestrial environment. Theme 3 also comprises two chapters and both
are associated with the application of indicators and surrogates in the measurement and
management of the atmosphere. Aquatic ecosystems are the core of the theme 4, with two
chapters featured. Theme 5 comprises three chapters on marine ecosystems. Theme 6 is
particularly fascinating as it contains two quite different kinds of chapters not normally
associated with the field of ecological indicators and surrogates. The first chapter in this
theme concerns the increasing use of genetic metrics and explores the exciting potential of
this relatively new area in the ecological surrogate domain. The second chapter in Theme
6 pivots around discussions of the learnings for the use of ecological indicators and surro-
gates in ecology that can be drawn from medical science and statistical science. Theme 7
comprises two chapters about indicators and surrogates in policy. The final theme 8 con-
tains just one chapter – an overview of learnings that come from the collected insights of
the chapter authors. In particular, what works well and what doesn’t, and what common
ideas can be used to guide future research on the selection and application of ecological
surrogates. This chapter was developed from the diversity of author experience and chap-
ter content, especially through a workshop held in south-east Queensland (Australia) in
October 2014.

Caveats and notes

As with any book comprising many topics written by different authors, there are some
inconsistencies in the approach and flavour of each chapter and the volume editors decided
that these could remain. The authors of each chapter were responsible for their own contri-
bution and only limited content editing was conducted. Of course we were acutely aware
that there are sometimes more than 10 key issues that could be considered in each sector,
ecosystem and cross-cutting theme. However, we felt that asking each author team to
highlight their ‘top 10’ was a good way to focus their writing around important insights
and key knowledge gaps that need to be filled.
A key concern we had at the commencement of this book writing project was the risk of
extensive overlap between chapters. In reality, there proved to be an impressive diversity of
topics, important synergies and limited overlap between chapters. We considered the little
overlap that did occur was tolerable because each chapter needed to be a stand-alone con-
tribution given the way many readers might ‘dip into and out of’ the book.
Ecological surrogates are likely to become even more important in guiding environ-
mental policy and management in future. Our sincere hope is that this book represents a
leap forward in the understanding and application of ecological surrogacy in terms of
breadth of expertise and examples, as well as the identification of core learnings that tran-
scend individual disciplines.
4 Indicators and Surrogates of Biodiversity and Environmental Change

References
Caro T (2010) Conservation by Proxy: Indicator, Umbrella, Keystone, Flagship, and Other
Surrogate Species. Island Press, Washington DC.
Collen B, Nicholson E (2014) Taking the measure of change. Science 346, 166–167.
Lindenmayer DB, Likens GE (2011) Direct measurement versus surrogate indicator species for
evaluating environmental change and biodiversity loss. Ecosystems 14, 47–59. doi:10.1007/
s10021-010-9394-6.
McGeoch MA (1998) The selection, testing and application of terrestrial insects as
bioindicators. Biological Reviews of the Cambridge Philosophical Society 73, 181–201.
doi:10.1017/S000632319700515X.
Niemi GJ, Hanowski JM, Lima AR, Nicholls T, Weiland N (1997) A critical analysis on the use
of indicator species in management. The Journal of Wildlife Management 61, 1240–1252.
doi:10.2307/3802123.
Rodrigues AS, Brooks TM (2007) Shortcuts for biodiversity conservation planning: the
effectiveness of surrogates. Annual Review of Ecology Evolution and Systematics 38,
713–737. doi:10.1146/annurev.ecolsys.38.091206.095737.
Westgate MJ, Barton PS, Lane PW, Lindenmayer DB (2014) Global meta-analysis reveals low
consistency of biodiversity congruence relationships. Nature Communications 5, 3899.
doi:10.1038/ncomms4899.
2

Surrogates for the distribution and trajectory of

biodiversity

Martin Westgate

Things we know
1 Most taxa show congruent distribution patterns.
2 Processes that influence congruence are scale-dependent.
3 Surrogate research is shifting towards species-level inference.
4 Functional ecology can help to identify biodiversity surrogates.
5 Surrogates should measure progress towards management goals.

Knowledge gaps
6 A long-term view of biodiversity surrogates.
7 Greater integration is needed across taxonomic boundaries.
8 Research on the mechanisms underpinning surrogate relationships is not
always worthwhile.
9 Complementary surrogates.
10 Adaptive surrogates.

Introduction
Biodiversity is a broad concept that encompasses several real and perceived values of eco-
systems. However, the idea that science can help to conserve biodiversity relies on the
assumption that biodiversity can be measured. Unfortunately, ecosystems are too complex
to allow comprehensive mapping of their specific or genetic diversity: only a small propor-
tion of all species have been taxonomically described, while data on species’ distributions
or risks of extinction are rarer still (Scheffers et al. 2012). Consequently, our ability to
measure ‘total’ biodiversity is dependent on surrogates: practical metrics that allow us to
identify locations or times where we find high numbers and/or distinct combinations of
species. In practice, most assessments of the distribution or trajectory of biodiversity rely
on information from a small number of frequently studied taxa, typically with an empha-
sis on vertebrate animals and vascular plants (Westgate et al. 2014). In this chapter, I will
refer to such metrics (i.e. those whose goal is the measurement of biodiversity) under the
umbrella term ‘biodiversity surrogates’. My aim is to explore the current state of the s­ cience

5
6 Indicators and Surrogates of Biodiversity and Environmental Change

of biodiversity measurement, discuss how a reliance on surrogates influences conservation

decisions, and suggest future directions for this important area of ecological research.

Things we know
1. Most taxa show congruent distribution patterns
A major component of biodiversity surrogate research involves the assessment of ‘congru-
ence’, which measures the extent to which information on one group of species provides
information on a second group. Perhaps the most common application of this approach is
to test the relationship between the spatial distributions of two distinct taxonomic groups
(known as ‘cross-taxon’ congruence). The success of this approach, and its utility for
informing conservation, varies strongly depending on a range of factors. In particular, dif-
ferences in how target and surrogate groups are defined and measured can strongly influ-
ence patterns of congruence (Rodrigues and Brooks 2007), as can attributes of study design
such as spatial scale or grain size (Westgate et al. 2014). Further, there is debate regarding
the extent to which different metrics for quantifying and comparing the diversity of two
groups provide useful information (see point 3 below). Therefore, caution must be taken
when using congruence-based approaches to infer patterns of biodiversity.
Despite these caveats, it is encouraging that the degree of congruence between taxa is
typically greater than zero, irrespective of the metric under investigation (Rodrigues and
Brooks 2007; Westgate et al. 2014). Pointing out that congruence is a common attribute in
nature is important because the academic literature is often highly critical of the surrogate
concept. Positive correlations occur between taxa because all life responds to similar pro-
cesses, particularly at large spatial and temporal scales. For example, studies of the influ-
ence of biogeographic parameters such temperature, latitude or elevation on taxonomic
diversity have a long history in ecology, and their respective influence on different taxa is
relatively well understood (e.g. Qian and Kissling 2010). This suggests that progress can be
made towards understanding patterns of congruence between different sets of species or
locations.

2. Processes that influence congruence are scale-dependent

Understanding the circumstances where we would expect to observe biodiversity congru-
ence would greatly assist conservation decision making. However, the number or diversity
of species at a given location is influenced by many processes, each acting at particular
spatial and temporal scales. For example, we still lack an overarching theory that describes
how evolution, species traits and species interactions combine to determine biodiversity at
macro scales (Nuismer and Harmon 2014). Moreover, much research on surrogates in
ecology and conservation focuses on how biodiversity responds to landscape-scale pro-
cesses such as disturbance or fragmentation, which are areas where cross-taxon synthesis
has traditionally been difficult (Ewers et al. 2010). These difficulties may explain why
many applications of the surrogacy concept lack a theoretical foundation, or are inconsist-
ent with known theoretical concepts (Sætersdal and Gjerde 2011).
Some authors have attempted to identify processes that influence cross-taxon congru-
ence across a range of spatial scales. In particular, groups of species that display strong
interactions such as predator–prey dynamics or mutualisms should be highly congruent,
but this does not always occur (Dehling et al. 2014). Alternatively, species may share physi-
ological attributes that ensure they display similar responses to climate or elevation, lead-
ing to high congruence (Hawkins and Porter 2003). Without a better knowledge of how
 2: Surrogates for the distribution and trajectory of biodiversity 7

these processes act and interact, however, we remain unable to predict when we should
expect sets of taxa to display high congruence.

3. Surrogate research is shifting towards species-level inference

Early attempts to identify biodiversity surrogates typically focused on correlations in spe-
cies richness and/or diversity across taxa, but prioritising locations with high species rich-
ness for conservation ignored areas with highest threat, or those with a high proportion of
endemic species (Orme et al. 2005). Further, many taxa display changes in species compo-
sition across ecological gradients, but not species richness (Supp and Ernest 2014). Conse-
quently, methods that use diversity indices to assess congruence have been largely
superseded by optimisation of species occurrences as the standard method for spatial pri-
oritisation (Williams et al. 2006). Similarly, hierarchical models are now capable of assess-
ing change in assemblage structure via logistic regression of individual species occurrences
(Wang et al. 2012), rather than relying on aggregate metrics. These tools have provided a
range of new insights into the distribution and trajectory of biodiversity.
This increased focus on species-level information, while encouraging, brings new chal-
lenges. First, species occurrence data are highly scale-dependent, with issues resulting
from spatial variation in species occupancy, abundance and detectability increasing at fine
scales (Hurlbert and Jetz 2007). Second, different software algorithms, or changes to the
underlying assumptions of the analysis, can lead to enormous differences in the ranking of
locations or actions for conservation (Grantham et al. 2010). Finally, applications of spatial
prioritisation can be more sensitive to the economic value of study units than to their bio-
logical composition (Bode et al. 2008): a property that is useful for efficient conservation,
but risks promoting the lesson that biodiversity itself is of secondary concern. Conse-
quently, care is needed when relying intensively on species-level datasets for conservation
decision-making.

4. Functional ecology can help to identify biodiversity surrogates

The functional approach to ecological research is based on the premise that knowledge of
species traits can be used to understand ecosystem structure. This concept is widely
accepted and studied, both because of its intuitive appeal (species differ from each other in
meaningful ways, and traits reflect that), and its usefulness for describing patterns in bio-
logical communities (models that ignore differences between species often perform worse
than models that account for those differences). Functional ecology is relevant to the sur-
rogate concept because it provides a robust mechanism that can explain patterns of co-
occurrence, and can therefore be used to identify reliable surrogates (Dehling et al. 2014).
While useful, however, several conceptual and practical issues remain in how species
traits are applied to biodiversity monitoring and management. In particular, the idea that
species traits mediate interactions between species, or between a single species and its
environment, is well accepted. Precisely which traits are used, however, and how they are
defined and measured, remains challenging. Unfortunately, learning about traits that
influence the distribution of plant species can rarely be transferred to understand patterns
in animals, and vice versa. Of those traits that can be compared across dissimilar taxa
(such as body mass, or related indices such as metabolic rates), controversy remains regard-
ing their mechanistic basis and degree of explanatory power (Isaac and Carbone 2010).
Further, work on animal traits remains largely descriptive, despite advances in predictive
science based on plant traits. For example, Lindenmayer and colleagues (2014) showed that
species selected for monitoring according to their traits did not occupy sites with high
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