Journal of ESSAY REVIEW

J.
Original
Blackwell
Oxford,
Journal
JEC
2006
0022-0477
94
TheSilvertown
Park Article
British
of
UK et al.
Publishing
Ecology
Ecological
Grass Ltd
Society
Experiment

Ecology 2006
94, 801–814 The Park Grass Experiment 1856 –2006:
its contribution to ecology
JONATHAN SILVERTOWN, PAUL POULTON*, EDWARD JOHNSTON*,
GRANT EDWARDS†, MATTHEW HEARD‡ and PAMELA M. BISS
Department of Biological Sciences, The Open University, Walton Hall, Milton Keynes, MK7 6AA, UK, *Rothamsted
Research, Harpenden, Hertfordshire AL5 2JQ, UK, †Agriculture Group, Field Services Centre, PO Box 84, Lincoln
University, Canterbury, New Zealand, and ‡Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton,
Huntingdon, Cambs. PE28 2LS

Summary
1 The Park Grass Experiment, begun in 1856, is the oldest ecological experiment in existence.
Its value to science has changed and grown since it was founded to answer agricultural
questions. In recent times the experiment has shown inter alia how: plant species richness,
biomass and pH are related; community composition responds to climatic perturbation
and nutrient additions; soil is acidified and corrected by liming. It also provided one of
the first demonstrations of the evolution of adaptation at a very local scale and contains
a putative case of the evolution of reproductive isolation by reinforcement. The appli-
cation of molecular genetic markers to archived plant material promises to reveal a
whole new chapter of genetic detail about the long-term dynamics of plant populations.
2 Over the range of values observed at Park Grass, biomass (productivity) has a negative
effect upon species richness. Any positive effect of species richness on productivity
could only be weak by comparison. The experiment provides support for both the
competitive exclusion and pool size hypotheses for determination of species density.
3 Instantaneous comparisons of species richness between plots do not accurately
reflect temporal rates of loss which may be multiplicative rather than additive. This
suggests that comparisons among sites, nutrient inputs, especially N treatments, or soil
acidity may in general underestimate the threat posed to plant species diversity by long-
term changes in plant nutrient availability, both enrichment and depletion.
4 Differences between plots at the community level are maintained despite a flow of
propagules between plots. There is no strong evidence for a spatial mass effect.
5 Guild (grass/legume/other) compositions of plant communities have equilibrated,
but the species composition within guilds is more dynamic and continues to change over
time, suggesting that species and guild abundances are independently regulated.
6 At least some members of all the major trophic levels, including predators (spiders), herbiv-
ores (leafhoppers) and detritivores (springtails) are treatment-specific in their distributions.
7 Plant populations on Park Grass are subdivided by treatments which, to some degree,
have led to plots becoming genetically isolated from one another and decoupled demo-
graphically. This subdivision has created a metapopulation structure in each species,
characterized by species-specific rates of local colonization and extinction.
8 Inverse clines in flowering time occur in the grass Anthoxanthum odoratum across
some plot boundaries. These suggest that reproductive isolation between plots has been
reinforced by natural selection.
9 Drift as well as selection may have taken place in A. odoratum, especially on plots where
effective population size is restricted by population bottlenecks caused by drought.
10 Park Grass illustrates how long-term experiments grow in value with time and how they
may be used to investigate scientific questions that were inconceivable at their inception.
© 2006 The Authors This is as likely to be true of the future of Park Grass as it has proved to be of its past.
Journal compilation
© 2006 British
Ecological Society Correspondence: Jonathan Silvertown (e-mail [email protected]).
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
802 Key-words: long-term experiment, permanent grassland, biodiversity, plant population
J. Silvertown et al. dynamics, natural selection, plant nutrition, soil fertility, stability, ecological genetics
Journal of Ecology (2006) 94, 801–814
doi: 10.1111/j.1365-2745.2006.01145.x

(Silvertown et al. 2005). Soil and hay samples from the

Introduction
experiment have been archived from the beginning and
The Park Grass Experiment (Fig. 1), begun by John B. these have been used in retrospective studies of atmos-
Lawes and Joseph H. Gilbert in 1856, at Rothamsted in pheric pollution (Zhao et al. 1998; Blake et al. 1999;
Hertfordshire, England, is the longest running ecological Warneke et al. 2002) and population genetics (Biss
experiment in the world (Tilman et al. 1994) and over et al. 2003). In the sections which follow, we provide a
170 publications have arisen from it to date. The early brief overview of the experiment, selectively review
results from Park Grass quickly answered the question results under the main topics of soil processes, plant
that motivated Lawes and Gilbert to start the experi- dynamics, evolution and fauna and then attempt to
ment, namely how different fertilizers would improve draw some of these threads together into a synthetic
the yield from hay meadows (Lawes & Gilbert 1859). overview that provides some general pointers for future
Today, Park Grass has acquired new relevance for the research.
study of fundamental ecological processes and for nature
conservation. It has inspired new ecological theory (the
The Park Grass Experiment
resource ratio hypothesis (Tilman 1982)) and has helped
ecologists to recognize the value of long-term experi-
  
ments in ecological studies, notably at Cockle Park in
Northumberland, UK (Arnold et al. 1976), Wageningen The site of the experiment is about 2.8 ha of almost
in the Netherlands (Elberse et al. 1983), Cedar Creek, level land that had certainly been in grass for more than
Minnesota, USA (Tilman 1987) and Nash’s Field, a century when the experiment began in 1856. The soil
Silwood Park, UK (Edwards et al. 2000). This paper was slightly acid (pH 5.4–5.6) and the nutrient status
aims to illustrate the modern relevance of Park Grass poor. The top 23 cm of soil is a silty clay loam overlying
and its unique and increasing value to various branches clay-with-flints and is moderately well drained. At the
of ecology. start, the species composition of the herbage appeared
In the temperate climate and on the silty clay loam uniform across the whole site. In terms of the modern
soil at Rothamsted, processes of soil development National Vegetation Classification (Rodwell 1992) the
and change are slow and require time to play out. Over vegetation of the meadow would have been mesotrophic
150 years the different treatments have variously resulted grassland of MG5 type (Dodd et al. 1994a).
in soil acidification, changes in soil organic matter, and P
and K enrichment or depletion, and these have all affected
   
the fragmentation of plant populations. Fortuitously,

some of these treatments have experimentally reproduced
two of the principle extrinsic impacts that threaten
Fertilizer and liming treatments
plant biodiversity in natural habitats more generally,
namely plant nutrient enrichment and acidification A plan of the experiment and amounts and forms of N,
of the soil, and therefore offer a unique opportunity P and K tested are given in Fig. 2, together with the
to study their long-term effects on extinction. The average nutrient content of the organic manures; more
numerous long-term treatments reveal relationships details are in Table S1 in the Supplementary Material.
between nutrient availability and grassland biodiver- Plots 1–13 were started in 1856; plots 14 –17 were added
sity (Silvertown 1980; Crawley et al. 2005). They have in 1858 while three others started later: plot 18 (1865) and
also provided a test of the influence of species richness 19 and 20 (1872). Before 1905, treatments to a limited
on the stability of plant communities in relation to number of whole plots were changed (Warren & Johnston
climate (Dodd et al. 1994b; Silvertown et al. 1994b) 1964). Since then, modifications have been made at various
that is highly relevant to the diversity–stability debate times by dividing the existing plots, but, the original
(Loreau et al. 2001). treatment has always continued on one subplot. A
A variety of patterns of long-term plant population regular application of lime on half-plots to test soil pH
dynamics related to life history have been discovered in effects was started in 1903 (Warren & Johnston 1964).
© 2006 The Authors
the experiment that are not detectable in shorter time By 1959 this liming had gradually created different pH
Journal compilation
© 2006 British
series (Dodd et al. 1995; Silvertown et al. 2002). Due to values in both the 0–23 cm and 23–46 cm soil depths
Ecological Society, its well-documented 150-year history, Park Grass is a for each treatment (Warren & Johnston 1964) (Fig. 3).
Journal of Ecology, fertile arena for the study of natural selection (Snaydon The difference in soil acidity with the various nutrient
94, 801–814 1970) and a promising subject for ecological genetics inputs had a major effect on species composition by 1964
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
803
The Park Grass
Experiment

Fig. 1 An aerial view of the Park Grass Experiment looking due north, taken on 23 May 2005. Note the sharp plot boundaries,
many of which are clearly demarcated by differences in vegetation.

(Thurston et al. 1976). Consequently, to extend the

Hay cutting and data collection
range of pH values, most plots were divided into four
subplots (a–d, Fig. 2) in 1965, with the aim of achieving Herbage has always been cut and made into hay on the
surface soil pH values of 7, 6 and 5 where possible by plots, usually in June. After hay harvest, the subsequent
applying appropriate amounts of lime, preserving the regrowth was grazed by sheep for 15 of the first 19 years;
fourth subplot as an unlimed control (Warren et al. since 1875 a second cut has been taken and removed
1965). Important modifications since then have tested from the plot. Thus, since 1875 species composition has
changes in nutrient inputs by dividing plots 9, 14, 13 not been affected by grazing.
and 2 (see Fig. 2 for details). Yields have been recorded, and samples kept for
Achieving and maintaining the desired pH in the surface analysis, from each plot and every harvest since 1856 and
soil on each subplot has taken many years, the rate of these data are lodged in the online Electronic Rothamsted
change has been variable and very different amounts of Archive (ERA: www.era.iacr.ac.uk/parkgrass_1.html).
lime have been required. The current pH of the top 23 cm Quantitative (weight of each species present in hay
of soil is given in Table S1. Soils with no nutrient inputs samples) and qualitative (presence/absence of species)
(unmanured) have changed little from an estimated value records of the botanical composition of plots have been
of 5.5 in 1856 (Fig. 3); the higher pH in 1923 compared to made at varying intervals. The first comprehensive, quan-
1876 is due to the small amount of lime added to all plots titative record was made in 1862 and then at 5-year
in the 1880s. The higher values on plots given sodium nitrate intervals until 1877. The most recent quantitative botanical
must be because sodium ions (Na+) have been lost as analyses on all plots were made annually between 1991
balancing cations in preference to Ca2+. Where N is applied and 2000 (Crawley et al. 2005). Numerous quantitative
as ammonium sulphate without lime, the soils have become surveys of subsets of plots were made between 1877 and
progressively more acid, reaching an apparent equilib- 1976 (Williams 1978). A separation of the hay by weight
rium at about pH 3.6. The same amount of chalk was into three guilds: grasses (Poaceae), legumes (Fabaceae)
added to soils receiving either ammonium sulphate or and ‘other species’ (non-legume, broadleaved herbs) was
sodium nitrate until 1964 (Fig. 3). After that date, the made annually for various plots for long periods between
NO3-N and the NH4-N plots required, respectively, 14 1858 and 1948 (Williams 1978; Silvertown 1987). Qual-
© 2006 The Authors
and 63 tha−1 CaCO3 in total between 1965 and 2003 to itative records of the presence/absence of species were
Journal compilation
© 2006 British
bring or maintain them both to pH 7 by 2000 (mean taken twice a year from every plot for 60 years between
Ecological Society, 1995–2005) (Fig. 3). The difference in the amount of 1920 and 1979 (Dodd et al. 1995) as well as less regularly
Journal of Ecology, chalk needed was due to the greater acidifying effect at other times before and since (Crawley et al. 2005).
94, 801–814 of ammonium sulphate. Botanical survey data are lodged in the ERA.
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
804
J. Silvertown et al.

Fig. 2 Plot layout and current treatments of the Park Grass Experiment.

ammonium sulphate and because of atmospheric N inputs.

Soil processes
Fertilizer N inputs have remained constant. However,
© 2006 The Authors
the input of atmospheric N (as wet and dry deposition)
Journal compilation   ,   
varies, both within and between years, depending on
© 2006 British 
Ecological Society, emissions to the atmosphere and rainfall. Goulding et al.
Journal of Ecology, Soil acidification has greatly affected species composition (1998) calculated that the annual atmospheric N input
94, 801–814 of the sward. Soils have acidified as a result of applying totalled c. 10 kg ha−1 at the start of the experiment,
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
805
The Park Grass
Experiment

Fig. 3 Surface soil, 0–23 cm, pH(in water) since 1856;
= plot 3 (unmanured);  = plot 14 (N*2PKNaMg);  = plot 14 plus chalk
since 1920;  = plot 9/2 (N2PKNaMg);  = plot 9/2 plus chalk since 1903.

increased gradually to c. 30 kg ha−1 by the 1960s before species composition will depend on the ability of plants
peaking at c. 45 kg ha−1 in the mid-1980s. Since then there to survive where there is so little plant-available P and
has been a decline to c. 35 kg ha−1. Acidification also K. Where P and K have been applied there is sufficient
occurs from inputs of sulphur dioxide which reached in the soil to meet the needs of any plant (Fig. 2).
a maximum of 65 kg S ha−1 each year in 1980 but have
since declined dramatically (McGrath et al. 2002) as a
Plant dynamics
result of declining emissions from industrial sources.

 
       
The various fertilizer treatments initiated in 1856 had
 
so dramatic an effect upon the botanical composition
Data from Park Grass has been crucial in extending the of different plots that Lawes & Gilbert (1859) wrote that
use of the soil organic matter model, RothC (Jenkinson in less than two years ‘the experimental ground looked
1990). Originally developed to look at the turnover of almost as much as if it were devoted to trials with
soil organic matter in the plough layer of arable soils, different seeds as with different manures’. Although the
organic C and 14C measurements on archived Park Grass initial changes were rapid, the communities continued
soils were used to demonstrate its validity for use in to change over the following 40 years, not reaching an
permanent grassland (Jenkinson et al. 1992). Additional equilibrium until the early 20th century (Silvertown
organic C and 14C analyses of recent and archived soils 1980; Dodd et al. 1994a). Even then, the equilibria were
sampled, by horizons, to a depth of 90 cm on Park only attained at the aggregate level (Micheli et al. 1999),
Grass and on arable and woodland sites are being used measured in terms of the proportions of grass/legume/
to further extend RothC such that the turnover of the other species (Fig. 4). These proportions were distinc-
very significant proportion of C stored in subsoils can tively different between treatments; grasses consistently
be taken into account. RothC and the Hadley Centre’s dominated (c. 90%) N-fertilized plots; legumes were
coupled climate–carbon cycle general circulation model abundant (> 30%) on plots receiving P and K but no N,
are now being used to predict the effects of global change and an intermediate ratio of the three guilds occurred
on soil carbon stocks (Jones et al. 2005). on unfertilized plots (Silvertown 1987).
In 2002, in the 0–23 cm soil layer of the unlimed soils While the guild composition of communities had
receiving no N or N as sodium nitrate (pH 5.0–5.6) equilibrated by 1910, the species composition within
there was 3.0% C, whilst those receiving ammonium guilds was more dynamic and continued to change over
sulphate (pH 4.1–3.6) contained 4.8–6.6% C. Most of time, suggesting that species and guild abundances
this difference is due to the accumulation of C in the mat are independently regulated (Silvertown 1980). Species
of undecomposed material on the most acid soils. This changes are discussed in a later section. The equilibrium
mat may affect the ability of the roots of germinating in guild composition is a dynamic one, continually
seeds to grow into the underlying mineral soil. Where perturbed by climate. Annual rainfall averages 698 mm,
soils have a pH of 6 or 7 a mat did not develop, or was but ranges widely from 380 mm in 1921 to 974 mm in
broken down, and percentage C is similar on all treat- 2000. Silvertown et al. (1994) found that above-average
ments, ranging from 3.7% to 4.2% C. spring rainfall directly increased hay biomass (see also
© 2006 The Authors
Current levels of plant-available soil phosphorus Cashen 1947), but altered guild proportions with a one-
Journal compilation
© 2006 British
(Olsen P) and potassium (exchangeable K) in the 0– year time lag, increasing grass abundance at the expense
Ecological Society, 23 cm soil layer are either very small or very large. On of the other two guilds. They suggested that the lag was
Journal of Ecology, soils not given P or K, Olsen P is about 4 mg kg−1 and the result of interspecific competition for light which,
94, 801–814 exchangeable K about 60 mg kg−1 (range 44–71) and because of positive feedback between growth and light
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
806 of community change depended upon soil pH. New com-
J. Silvertown et al. munities differed from those on plots that had the same
current fertilization treatment, but no history of pertur-
bation. This is an important observation: halting the
application of N while leaving soil acidity uncorrected is
unlikely to cause any major change in sward composition.

   


The clear effects of different fertilizer treatments on plant
community composition in the Park Grass Experiment
were used by Tilman (1982) in support of the resource
ratio hypothesis when he gave the hypothesis its first
full exposition. The hypothesis proposes that the number
and relative abundances of plant species in a community
at equilibrium are determined by competition for essential
resources such as plant nutrients and light. All plant
species require a common suite of such resources, but
each species has its own characteristic ratio of essential
resources at which resource availability limits growth.
According to the hypothesis, when two or more species
consume the same essential resource the winner in the
competition for that resource will be the one able to toler-
ate (i.e. continue growing at) the lowest concentration.
In general, legumes, such as Lathyrus pratensis for
example, can continue to grow at a lower resource con-
centration of N than can grasses such as Agrostis tenuis.
When supplied with sufficient N, grasses have the upper
hand against legumes in competition for P. Thus, grasses
dominate N-fertilized communities like Plot 14 (Fig. 4a)
while legumes are favoured in Plot 7 (Fig. 4b) that receives
P, but no N. Coexistence is possible in intermediate situ-
ations if there is spatial heterogeneity in N : P ratios.
Tilman’s (1982) graphical application of the resource ratio
hypothesis to competition between L. pratensis and A.
tenuis in Park Grass plots is reproduced in Fig. 5(a).
Tilman (1982) also proposed that differences between
Park Grass communities in the relative abundances of
four grasses and L. pratensis could be explained by the
Fig. 4 Relative proportions by dry weight annually between resource ratio hypothesis if the species’ relative require-
1910 and 1948 of grasses (white), legumes (light grey) and ments for light and N were negatively correlated. This
other broad-leaved herbs (dark grey) on un-limed sections of
trade-off is indicated by the ranking on axes for light and
plots receiving (a) N*, P, K, Na and Mg; (b) P, K, Na and Mg;
(c) no fertilizer. Proportions in 1975 and 1976 are shown for N of zero net growth isoclines in Fig. 5(b). The isoclines
comparison. (after Silvertown 1987; with permission and and consumption vectors shown in Fig. 5 and in the many
redrawn with data from the Electronic Rothamsted Archive). other Park Grass examples used by Tilman (1982) are
hypothetical, but are consistent with observations made
capture, would amplify climatic effects on grass growth in the experiment. Despite two decades of research inspired
and thereby increase the competitive suppression of by the resource ratio hypothesis (Craine 2005), a recent
legumes and other species. Dunnet & Grime (1999) review (Miller et al. 2005) concluded that important work
subsequently demonstrated such an amplification effect remains to be done in measuring isoclines and consump-
in experimental grassland microcosms. tion vectors in the field in order to test the hypothesis fully.
Changes in fertilizer treatment on plots that have
recently been split (see section ‘Experimental treatments
© 2006 The Authors 
and management’) have afforded the opportunity to
Journal compilation
© 2006 British
observe how quickly grassland communities change in
Determinants of species richness
Ecological Society, response to a ‘press’ type of perturbation (Bender et al.
Journal of Ecology, 1984). Comparing subplots where N fertilization had The relationship between species richness and produc-
94, 801–814 ceased with controls, Henman (2001) found that the speed tivity has been the subject of heated debate (Huston
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
807 tive manner (Silvertown 1980). By the 1990s plots acidified
The Park Grass by fertilization with ammonium sulphate had lost so many
Experiment species that they no longer showed variation in species
density in response to biomass (Crawley et al. 2005).
All plots, including the unfertilized ones, have lost
species with time (Silvertown 1980). On non-acidified
plots, for example, about 18 species per plot were lost
over the 130 years from 1862 to 1991 (Dodd et al. 1994b).
Some loss due to the subdivision of plots might be
expected, but species–area relationships suggest that a
plateau is reached at 75 m2, which is the smallest plot
size (Crawley et al. 2005). Other possible causes of
widespread species loss are external. These include
varying degrees of soil acidification, inputs of N and S
as manures, fertilizers and from aerial deposition, and
soil enrichment or depletion of P and K. On plots where
soil pH remained at or above its estimated starting
value, because of treatment or liming, acidification cannot
have been a cause of species loss.
According to the multivariate model of species density
variation of Crawley et al. (2005), 50 kg N ha−1 year−1
added as fertilizer reduces species number by about 6.5
species, compared to the no N plots. Since the start of
the experiment, N-deposition slowly increased to reach
a maximum of c. 45 kg N ha−1 year−1 to all plots in the
1980s but the amount is now nearer 35 kg N ha−1 year−1.
This input alone could therefore account for a significant,
experiment-wide loss of species. Such an effect has
already been demonstrated for acid grasslands in the
UK (Stevens et al. 2004).
Note, however, that the model predicts only about a
third of the species loss that was actually observed between
1862 and 1991. This could be because the model is based
upon between-plot variation in the 1990s, while the total
loss of species took place over the previous 130 years
Fig. 5 Application of the resource ratio hypothesis to competition when species number was greater. This difference could
(a) for P and N between Lathyrus pratensis and Agrostis tenuis be important for three reasons. First, the most vulnerable
and (b) for light and N between L. pratensis and the grasses A. species may already have been lost by the 1990s. We may
tenuis, Dactylis glomerata, Festuca rubra and Holcus lanatus. call this a ‘sensitivity effect’, and it would result in a
Thin lines are zero net growth isoclines and thick lines are
consumption vectors for species. Arrows indicate compositional
lower rate of species loss caused by N addition in the 1990s
change caused by nutrient addition from the starting point on than previously. The existence of a sensitivity effect is
unfertilized control plots 3 and 12 towards the composition in supported by the results of Dodd et al. (1994b) who
1948/49 of communities on the fertilized plots indicated. In found that the slope of the species richness vs. biomass
(b), light availability at the soil surface was assumed to decline relationship on non-acid plots was significantly steeper,
as biomass increased with N-fertilization (from Tilman, 1982;
with permission, Princeton University Press).
by 30%, in 1862 than it was in 1991.
The detected effect might explain some of the difference
between modelled and expected species losses, but the
observed discrepancy is very large and other explanations
1997; Loreau et al. 2001). The Park Grass data show should be considered. A second reason for the discrepancy
unequivocally that, over the range of values observed, could be that the model used only the amount of fertilizer
biomass (productivity) has a negative effect upon species N applied. However, atmospheric and soil derived N (which
richness (Crawley et al. 2005). Consequently, any positive could vary with past treatment and soil pH) could have
effect of species richness on productivity could only be increased the total amount of N available to the herbage
weak by comparison, or can occur only in very different in any one year. The third and perhaps a more important
© 2006 The Authors
circumstances to those prevailing in mesotrophic grass- consideration is that instantaneous comparisons of
Journal compilation
© 2006 British
land (Keddy 2004). Modern species numbers vary from species richness between plots do not accurately reflect
Ecological Society, 3 to 44 per 200 m2 among the plots (Crawley et al. 2005). temporal rates of loss which may be multiplicative rather
Journal of Ecology, Historically, the primary determinants of this variation than additive. This is an important possibility because it
94, 801–814 were hay biomass and soil pH, which operated in an addi- suggests that comparisons among sites or N treatments
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
808
J. Silvertown et al.

Fig. 6 Metapopulation dynamics of some representative species on non-acidified plots of the Park Grass Experiment: (a) increase
in Trifolium pratense; (b) decrease in Veronica chamaedrys; (c) outbreak in Tragopogon pratensis; and (d) fluctuation in
Conopodium majus. From Dodd et al. (1995).

may in general underestimate the threat posed to plant specific rates of local colonization and extinction. Dodd
species diversity by long-term changes in plant nutrient et al. (1995) discovered that between 1920 and 1979
availability, both enrichment and depletion. some species occurred in increasing numbers of plots,
some declined and another group which they called
‘outbreak’ species first increased and then decreased
Diversity and stability
again (Fig. 6). Comparing the two groups of species that
The long-established differences in species diversity initially increased (i.e. the increasers and outbreakers)
between adjacent plots and the very long time series with species that did not change, the former were
of data on hay biomass make the experiment an ideal more ruderal (sensu Grime et al. 1988) than the latter.
system in which to address the long-debated question Silvertown et al. (2002) suggested that the initial increases
of how diversity and stability are related (May 1973; were triggered by drought which reduced interspecific
Tilman & Downing 1994). Plots with low biomass (which competition, allowing more ruderal species to increase
also tend to have greater species richness) and the acid and confirmed experimentally that the outbreak species
plots have the most variable hay biomass (Dodd et al. had a higher net reproductive rate than other species
1994b). Dodd et al. (1994b) regressed the variability of when released from competition.
hay biomass, measured in an 11-year moving window, Among the two groups that initially increased, Dodd
upon biomass itself and species number per plot for 42 et al. (1995) found that those species that decreased
different years between 1862 and 1991. In many years again (the outbreakers) had selfing mating systems when
(29/42) species richness was positively correlated with compared with the increasers that were able to sustain
stability of hay biomass, although the correlation was themselves on plots that they had colonized. This
significant in only three years. Species richness may correlation with mating system was confirmed by
therefore have some stabilizing effect upon hay biomass, Silvertown et al. (2002) who estimated selfing rates in
but the effect would appear to be weak. populations on Park Grass and found that, as expected,
outcrossing and genetic diversity were positively cor-
related. Silvertown et al. (2002) proposed that selfing
  
species may have declined after their initial spread
Plant populations on Park Grass are subdivided by because of one or more ecological handicaps created by
© 2006 The Authors
treatments which, to some degree, have led to plots selfing: inbreeding depression, an inability to adapt to
Journal compilation
© 2006 British
becoming genetically isolated from one another (see the environment of new plots because of limited genetic
Ecological Society, section ‘Evolution’, below) and decoupled demograph- variation, or susceptibility to pathogens.
Journal of Ecology, ically. This subdivision has created a metapopulation These ideas have not yet been tested, though the
94, 801–814 structure in each species, characterized by species- outbreak species Tragopogon pratensis, which has no
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
809 detectable genetic variation, is highly susceptible to
The Park Grass rust disease. Results from an annual sampling of plant
Experiment density and rust infection from 1995 to 1998 and 2000–
04 (G.R. Edwards et al., unpublished data), showed that
within years, there was a significant negative correlation
between plant density per plot and percentage rust
infection in 4 of 9 years. In 4 out of 7 years there was
a significant correlation between the severity of rust
infection on plots and a decrease in plant density the
following year. These results suggest the operation
of delayed density dependence which might cause
population cycling or even chaotic dynamics.

Evolution

  
The classic study by Snaydon & Davies (1972, 1976, 1982;
Snaydon 1970; Davies & Snaydon 1973a,b, 1974, 1976)
of evolution in Anthoxanthum odoratum growing on Park
Grass plots was an early demonstration of the now Fig. 7 Time series, 1870 –2000, of Anthoxanthum odoratum
abundance (t ha−1 dry matter) on plots with contrasting pH
well-known tendency towards local adaptation in plants (measured 1995–2005).
(Linhart & Grant 1996). Even though A. odoratum is
outcrossing (self-incompatible) and wind pollinated and
therefore considerable gene flow across plot boundaries Local adaptation has been tested in only one other
must occur, heritable differences in many traits were plant species found on the plots, Holcus lanatus. Naylor
found between closely adjacent populations growing et al. (1996) tested for the frequency of arsenate tolerance
on the plots receiving different treatments. Reciprocal on different plots but found no correlation with soil
transplants between plots receiving different treatments conditions. In a glasshouse study, no differences between
demonstrated that selection coefficients against non- H. lanatus growing on a plot with (14/2c) or without
native genotypes could be over 70%, based on plant (15c) N fertilizer was found for root growth, overwinter
survival over an 18-month period (Davies & Snaydon seedling survival or leaf shape (F. van denBerg, pers.
1976). comm.). Why one species, A. odoratum, should show
Snaydon & Davies (1976) found heritable flowering local adaptation in many traits while another, H. lanatus,
time differences between plants on adjacent plots that exposed to the same selection pressures does not is
could potentially reduce gene flow. At the boundary unclear. However, this situation is quite common
between the then limed halves of plots 8 (pH 7) and 9 (Bradshaw 1991), and Park Grass is well suited to its
(pH 5.3) there was an inverse cline in flowering date, further investigation.
with plants on the border flowering several days earlier
than those either side. Over 30 years after Snaydon and
 
Davies’ samples were collected, Silvertown et al. (2005)
found an inverse cline in flowering time on the border Drift as well as selection may have taken place at Park
between the unlimed d subplots of plots 8 and 9/1. There Grass, especially on plots where effective population
was also significant genetic differentiation at ISSR marker size (Ne) is restricted by population bottlenecks. In a
loci between populations either side of the boundary and fluctuating population, Ne is approximately equal to
genetic evidence of greatly reduced gene flow via pollen. the harmonic mean of effective population size in each
Silvertown et al. (2005) suggested that reproductive separate generation (Wright 1969). Low values have a
isolation across the boundary between plots 8d and 9/ highly disproportionate effect upon a harmonic mean,
1d had been reinforced by natural selection. and so a population crash caused by drought has the
Reinforcement is a controversial evolutionary potential to create a genetic bottleneck that will leave
mechanism that may facilitate sympatric speciation. an imprint upon genetic structure long after the popu-
Few, if any, incontrovertible examples from the field are lation has recovered its former abundance. Very acid
known (Servedio & Noor 2003). A critical requirement plots, such as plot 9/2d (pH 3.8), have the greatest
for reinforcement to occur is that hybrids between variance in biomass (Dodd et al. 1994b) and so ought
© 2006 The Authors
populations should have lower fitness than within- to be the most susceptible to the loss of genetic variation
Journal compilation
© 2006 British
population crosses. This is yet to be tested at Park Grass, through drift (Fig. 7).
Ecological Society, but seems highly likely given the very strong selection Chloroplast microsatellite markers (Biss et al. 2003;
Journal of Ecology, against alien genotypes demonstrated by Davies & Provan et al. 2004) were used to haplotype leaves of
94, 801–814 Snaydon (1976). Anthoxanthum odoratum from archived hay samples
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
810 taken from the crops on Plots 8d (pH 5.2), 9/2d (pH 3.8)
J. Silvertown et al. and 12d (pH 5.2) and from fresh leaves sampled from
these plots in 2001. Between 1870 and 2001 haplotype
diversity (measured by the Shannon information function
H′) more than halved on plot 9/2d, while on the less
variable plots 8d and 12d it did not change significantly.

Fauna
The degree to which species in one trophic level influence
the composition and abundance of species in other
trophic levels is an active area of ecological research
(Hunter & Price 1992; Shurin et al. 2006). Variation in Fig. 8 Relationship between log10 total insect herbivore number
plant species composition among plots has been used and species richness across plots (F1,15 = 6.08, P < 0.05;
R2 = 29%).
as a basis for investigating bottom-up (plant → herbivore)
effects at Park Grass. Morris (1992) sampled the
Auchenorrhynca (leafhoppers) of 13 pairs of b and d
subplots at Park Grass and found that the species com- ecosystem hypothesis’ (EEH) developed by Oksanen
position of this group varied with amounts of applied et al. (1981) suggests that the intensity of herbivory varies
N and soil pH. The species richness of Auchenorrhynca, systematically with productivity because of increasing
though not their total abundance, was correlated positively top-down control at higher productivities, and predicts
with soil pH and negatively with N fertilization. Since peak herbivore impact at intermediate levels. Thus
plant and leafhopper species richness were affected by many factors can affect insect herbivore impact. These
N and pH in the same direction, this suggests that plant are rarely addressed simultaneously in field studies, but
species number may be the underlying cause of variation this has been done for insect herbivores in the Park
in herbivore species number, although Morris (1992) did Grass Experiment by Heard (1999).
not measure the direct correlation between these variables. Heard (1999) used field observations of insect
Edwards et al. (1976) did find a direct positive abundance and herbivore damage to pot individuals
correlation between the species richness of plants and (phytometers) of five plant species (two grasses and three
Collembola (springtails). Collembola are mostly detri- forbs), introduced into the plots to test the various
tivores, so the link between their diversity and plant hypotheses. As expected, results showed considerable
species richness may be indirect. Edwards et al. (1976) variation in intensity of herbivory (0–74% leaf area)
found that the total spider fauna at Park Grass included across plant species. In general, damage decreased with
species normally associated with several different grassland increasing neighbourhood plant species richness (F1,16 =
types, reflecting the heterogeneous nature of the vegeta- 5.11, P < 0.05), consistent with EH. More detailed
tion. However, the effects of specific plot treatments on the observations on Ranunculus acris showed that mean leaf
surface invertebrates sampled by Edwards et al. (1976) damage per plot decreased with increased plant diversity
were weaker than those affecting the Auchenorrhynca (Shannon–Weiner index, F1,12 = 6.32, P < 0.05; R2 = 35%),
studied by Morris (1992). also supporting EH. However, there was also partial
The range of plant communities in the Park Grass support for EEH because increased plant productivity
Experiment allows hypotheses predicting how plant resulted in increased intensity of leaf damage although
communities affect insect abundance and in particular there was no sign of a hump in the relationship. In
the intensity of herbivory to be tested. Two different but contrast, the effect on Rumex acetosa phytometers pro-
not mutually exclusive hypotheses reflect observations vided support for both the EH and RCH hypotheses.
that insect herbivore loads are reduced in more diverse Insect sampling showed decreased herbivore abundance
plant assemblages (Root 1973). The ‘resource concentra- with increased plant species richness (Fig. 8) also
tion’ hypothesis (RCH) predicts that insect herbivores consistent with EH. Whilst the study demonstrates
are more likely to find and remain in areas where their systematic variation in invertebrate herbivory across
host plants are concentrated in time and space. The community types, there was little evidence that one
‘enemies hypothesis’ (EH) predicts that natural enemies hypothesis satisfactorily accounts for the whole range
of insects are expected to be more abundant in polycultures of variation observed. The herbivores of some plant
and thus suppress herbivore population densities more species obviously have highly individualistic responses
efficiently than in monocultures. Both predict higher to habitat variables. The impacts of plant species richness
herbivore densities in monoculture but differ in their and productivity are clearly important, but the negative
© 2006 The Authors
predictions for polyphagous herbivores. In the ‘micro- correlation between these parameters among Park Grass
Journal compilation
© 2006 British
climate hypothesis’ differences in the structural plots makes it difficult to separate their relative impacts
Ecological Society, complexity of vegetation affect microclimate and may alter and importance. Further analysis of the invertebrate
Journal of Ecology, herbivore abundance through lowered mortality rates or food web structure may elucidate the impacts on the abun-
94, 801–814 increased fecundity (Crawley 1983). The ‘exploitation dance and relationship of specific functional groups.
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
811 The soil fauna at Park Grass is strongly influenced by N (Crawley et al. 2005). One way in which biomass
The Park Grass by N treatment and pH and its variation among plots reduces species richness is by limiting seedling recruitment
Experiment has ecosystem effects. In particular, earthworm density (see above). The pool size effect is seen most clearly in
decreased with increasing levels of N application and the effect of pH on species richness. Few species in the
with decreasing pH (Edwards & Lofty 1975). On soils with Rothamsted flora, other than Anothoxanthum odoratum
pH 4 and below, earthworms were absent. Earthworms and Holcus lanatus, can tolerate the high levels of
perform an important ecosystem function by burying plant-available aluminium found on the very acid plots.
dead leaf material on the soil surface. The absence of Decreases in soil pH lower species richness and operate
earthworms and decreased microbial activity on the most additively with the effect of biomass (Silvertown 1980).
acid plots (e.g. plot 9/2d), has led to the accumulation These results are relevant to recent debates on the func-
of a layer of undecomposed, peat-like organic matter on tional role of species diversity in plant communities.
the soil surface. The failure of plant roots to penetrate They indicate that in mesotrophic grasslands produc-
from the organic layer into the mineral soil underneath tivity will suppress species diversity rather than species
appears to be the cause of the severe drought sensitivity diversity promoting productivity. Species diversity also
of plant populations on plot 9/2d (Fig. 7). has a minimal effect on the variance of biomass over
years (Dodd et al. 1994b). Invertebrate communities at
Park Grass merit further study, but the results discussed
Discussion
indicate that at least some members of all the major
The Park Grass Experiment is unique, not just because trophic levels, including predators (spiders), herbivores
of its duration but also because of the range of investi- (leafhoppers) and detritivores (springtails) are plot-
gations that have been carried out there. Even though specific in their species distributions. In most cases the
different investigators have pursued independent lines distribution of invertebrates is probably related to either
of enquiry, the cumulative result has the potential to the species composition or the physical structure of the
tell us about more than the sum of the parts. Before a vegetation. Either mechanism might cause climate-driven
synthesis is attempted, what have we learned about the changes in the vegetation to propagate upwards through
parts? First, that the plant communities in the experiment the food web. Voigt et al. (2003) found that higher trophic
are at dynamic equilibrium (Silvertown 1987), where levels were more sensitive to climate than lower ones in
the average guild structure of the vegetation on a plot is grassland communities. Park Grass would be an ideal
determined by nutrient availability, particularly N, but system in which to investigate tritrophic interactions and
also P and K, and lime, and is continually perturbed by the degree of coupling between trophic levels over time.
climate (Silvertown et al. 1994). Although there is an In at least one very important case fertilizer treatment
equilibrium at the guild level, individual species within has had a direct effect. Lack of microbial activity and
guilds change abundance and distribution among plots the absence of earthworms on the very acid soils given
in a more dynamic manner which is at least partly related ammonium sulphate and not limed has led to the devel-
to species’ life-history traits (Dodd et al. 1995; Silvertown opment of a surface mat of peat-like material that is a
et al. 2002). Some of the changes within plots may few centimetres thick. This mat is greatly affected by
also be driven by changes in the availability of nutrients both freezing and drought which, in turn, has had an
(Tilman 1982). For example, Taraxacum officinale effect on the species growing on these soils. These are the
responds strongly to K and liming (Tilman et al. 1999). two grasses, Holcus lanatus and Anthoxanthum odoratum,
The potential for compositional change, some of which and their susceptibility to drought can, in some years,
is held in check by regulatory processes, is further illus- produce a population bottleneck (Fig. 7). The causal
trated by the fact that seedlings of certain species turn relationships between fertilizer treatment, soil pH, micro-
up in plots (e.g. Taraxacum officinale and Rumex bial activity and earthworms, drought and population
acetosa in 18d) where adults of the species are absent bottlenecks illustrates one way, amongst many possible
(G.R. Edwards, unpublished data). Even though seeds ways, that Park Grass studies lend themselves to synthesis
disperse across plot boundaries, this does not result (Fig. 9). The preliminary evidence on chloroplast
in any strong spatial mass effect altering community haplotype variation presented in an earlier section
composition at plot edges (Kunin 1998). Just as at the suggests that population bottlenecks caused by drought
population level genetic differentiation between plots on highly acidified soils may lead to loss of genetic
has occurred in spite of gene flow, differences between variation through drift.
plots at the community level are maintained despite a What the long-term consequences of this may be for
flow of propagules between plots. Park Grass is perhaps plant population viability in a world where extreme
the clearest example there is of the need to study com- climatic events are predicted to recur with increasing
munity variability at a hierarchy of levels (Micheli et al. frequency (Meehl & Tebaldi 2004), we do not yet know.
© 2006 The Authors
1999). Second, we have learned that the Park Grass One scenario is that genetic bottlenecks can tip a
Journal compilation
© 2006 British
Experiment provides support for both the competitive population into an extinction vortex if effective popu-
Ecological Society, exclusion and pool size hypotheses for determination of lation size (Ne ) and census population size are coupled
Journal of Ecology, species density. Species richness is negatively correlated by positive feedback (Frankham 2005). The archive of
94, 801–814 with total plot biomass, which is itself controlled mainly hay samples at Park Grass contains genetic material
 13652745, 2006, 4, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.1365-2745.2006.01145.x, Wiley Online Library on [27/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
812
J. Silvertown et al.

Fig. 9 A schematic model of the proposed mechanism by which climatic variation in rainfall, mediated by the influence of plot
treatment on soil invertebrates and of these on soil structure and hence soil moisture, influence plant abundance and population
genetic structure (Ne).

belonging to multiple populations that have gone locally presence of the kind of powerful effects of soil nutrients
extinct during the history of the experiment, offering and climate shown at Park Grass remains to be seen.
the possibility that the genetics of recorded extinctions The first 150 years of the Park Grass Experiment
could be analysed retrospectively. have taught us a great deal, but there are still whole
Synthesizing the results from another perspective, parts of the communities it contains, like the fungi, that
Park Grass is of increasing relevance to grassland have yet to be studied and there are many unanswered
management for nature conservation. The experiment questions. These gaps notwithstanding, if ecosystems
now contains several grassland types recognized by the are like multidimensional jigsaw puzzles, then Park
National Vegetation Classification, including remnants Grass is beginning to show us what the picture on the
of the original MG5 hay meadow which is now a grass- lid of the box must look like. This should provide a
land type that is an object of conservation efforts in its useful crib for those trying to solve similar ecological
own right. Nutrients and soil pH control community puzzles in other grassland ecosystems.
composition and species diversity and there are
regulatory mechanisms that keep these in equilibrium,
Acknowledgements
but these equilibria can be shifted to new positions. A
changing climate could potentially do this because its We are grateful to the Lawes Agricultural Trust for
effects can be amplified by interspecific competition. permission to work on Park Grass and to NERC and
This implies the possibility of rapid community change the Open University for funding. Rothamsted Research
in future, causing a decrease in species diversity. receives grant-aided support from the UK Biotechnology
Significant numbers of species have been lost from all and Biological Sciences Research Council. We thank
Park Grass plots. We can account for a proportion of David Henman for contributing to the drafting of the
these losses through the effects of nutrient treatments, paper and four anonymous referees for comments.
acidification and the traits that make certain species
more vulnerable than others, but it is worrying that
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© 2006 The Authors

Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 801–814