OIKOS 96: 421–432, 2002
Are differences in seed mass among species important in
structuring plant communities? Evidence from analyses of spatial
and temporal variation in dune-annual populations
David A. Coomes, Mark Rees, Peter J. Grubb and Lindsay Turnbull
Coomes, D. A., Rees, M., Grubb, P. J. and Turnbull, L. 2002. Are differences in seed
mass among species important in structuring plant communities? Evidence from
analyses of spatial and temporal variation in dune-annual populations. – Oikos 96:
421–432.
We analyse the population and spatial structures of coastal annual-plant communities, across ten dunes and three years, to explore the role of seed mass in structuring
these communities. One suggestion is that annual-plant communities are structured
by competition-colonization trade-offs driven by difference among species in seed-allocation strategies, while another perspective is that seed mass influences the ways in
which species respond to environmental variation. In support of the competition-colonization trade-off, the two largest-seeded species found on the dunes (Erodium
cicutarium and Geranium molle) were negatively associated with the other guild
members at the 10-mm scale in 1995, suggesting they locally excluded smaller-seeded
species in that year (when population densities were high). In support of the
environmental response hypothesis, populations of annual plants declined between
1995 and 1996 on eight of the ten dunes, underscoring the importance of year-to-year
environmental fluctuations in determining population sizes. The species that became
relatively uncommon also became more aggregated in space, and this effect was most
pronounced among the small-seeded species. Thus, small-seeded species may be
forced to retreat into refuges when conditions are unfavourable, where reduced
frequencies of interspecific contacts may increase their chances of persistence. We
also show that small-seeded species sometimes reach much higher population densities than larger-seeded species, consistent with earlier findings, but reason that this
abundance/seed mass relationship could have resulted from either a competition-colonization trade-off or from different responses of small- and large-seeded species to
environmental variation. We conclude that dune-annual species with contrasting seed
masses respond differently to environmental variation, while the competition-colonization trade-off plays a lesser role in community dynamics than previously considered.
D. A. Coomes and P. J. Grubb, Dept of Plant Sciences, Uni6. of Cambridge, Downing
Street, Cambridge, UK CB3 2EA ([email protected]). – M. Rees and
L. Turnbull, Dept of Biology, Imperial College at Silwood Park, Ascot, Berkshire, UK
SL5 7PY.
Over the last 30 years, population ecologists have made
substantial advances in understanding the ways in
which density-dependent and density-independent factors determine the dynamics of annual plants (Harper
1977, Watkinson et al. 2000). Yet little is known about
the ways in which these populations of annual plants
interact with one another within communities (Law and
Watkinson 1989, Rees et al. 1996). One perspective is
that simple rules underpin community dynamics. For
example, Rees (1995) has argued that seed mass is very
important in structuring the dynamics of dune-annual
communities, basing his arguments on the following
Accepted 20 September 2001
Copyright © OIKOS 2002
ISSN 0030-1299
OIKOS 96:3 (2002)
421
reasoning: (a) plant species have limited resources available for seed production, and therefore must trade off
the advantages of producing numerous seeds against
producing fewer larger seeds (Turnbull et al. 1999,
Jakobsson and Eriksson 2000), (b) experiments in
glasshouses show that large-seeded species are strong
competitors because of their size advantage, while (c)
small-seeded species are better colonizers, because some
of the many seeds produced will land in suitable
patches. Hence Rees (1995) reasoned that differences in
seed-allocation strategies are responsible for competition-colonization trade-offs among annual plants.
Many theoretical studies have investigated the competition-colonization trade-off, demonstrating that it provides a mechanism by which species may coexist
indefinitely in communities (Skellam 1951, Armstrong
1976, Tilman 1994).
Another school of thinking maintains that life-history traits are not important per se, but that the
differential responses of species to environmental variation provide a mechanism for coexistence (e.g. Grubb
1977, Grubb et al. 1982, Chesson 1985, Bonis et al.
1995, Higgins et al. 2000). For example, detailed observations of the demographics of Bromus tectorum (Mack
and Pyke 1984) showed the annual grass to be highly
influenced by year-to-year variation in environment,
leading the authors to conclude that the ‘‘characterisation of any species … on the basis of life history traits
alone may be erroneous’’. This school argues that fluctuations in the population densities, such as those observed on dunes and chalk grasslands (Grubb et al.
1982, Grubb 1986), reflect the differential responses of
species to year-to-year environmental variation. Few
ecologists would dispute that year-to-year variation in
environmental conditions can exert a large influence on
population densities, but it remains contentious
whether these fluctuations promote coexistence (Shmida
and Ellner 1984, Chesson 1985). Seed mass could be an
important attribute in determining species responses to
environmental variation – several studies show that
small-seeded species are more susceptible to death as
seedlings under unfavourable conditions such as periods of drought (Watkinson 1981, Crawley and
Nachapong 1985, Mazer 1989, Leishman and Westoby
1994, Leishman et al. 2000).
What methods are available for exploring these contrasting perspectives? One approach is an analysis of
overall patterns of abundance. Rees (1995) showed that
small-seeded species sometimes (but not always) reach
much higher population densities than larger-seeded
species on sand-dunes (see also Guo et al. 2000a). He
argued that these observations were consistent with his
trade-off theory, because simulations of the competition-colonization trade-off produce negative relationships between seed mass and abundance when
larger-seeded species are strongly dispersal limited (M.
Rees unpubl.). However, it can also be reasoned that
422
such patterns are generated by year-to-year environmental variation: Small-seeded species have the potential to become numerically dominant if climatic events
are favourable for them, because of their high per-capita seed production (e.g. Turnbull et al. 1999, Jakobsson and Eriksson 2000), but in many years they are
knocked back by unfavourable conditions (Watkinson
1981). In contrast, large-seeded species such as Vulpia
fasciculata have low per-capita seed production (Harper
1977), and so are incapable of rapid population growth,
even in favourable years.
A second tool for understanding community structure is the analysis of spatial patterns. Analyses of the
spatial arrangements repeatedly demonstrate that
herbaceous communities are non-random on the scales
at which competitive processes are likely to occur
(Greig-Smith 1952, Mahdi and Law 1987, Pacala and
Silander 1990, Herben et al. 1993, Law et al. 1993, Cain
et al. 1995). Even the ‘simple’ competition-colonization
trade-off can produce complex spatial structure, as a
result of local competitive interactions and dispersal
(e.g. Lehman and Tilman 1997), and this spatial structure can in turn have important implications for community dynamics (Pacala 1986, Pacala and Deutschman
1995, Bolker and Pacala 1999). In contrast, very little is
known about whether environmentally induced fluctuations in population sizes are accompanied by systematic
changes in spatial pattern (Guo et al. 2000b), but such
spatial-temporal covariance could also be very important for community dynamics. For example, if species
become more aggregated in years of rarity, provided
the patches are non-coincident, then they could become
less exposed to competition from other species, thereby
increasing their chances of persistence (Harper 1977,
Pacala and Levin 1997). Therefore it is important to
establish patterns of spatial aggregation and covariance.
This paper explores spatial structure and abundance
patterns with the objective of exploring the role (if any)
that seed mass plays in structuring annual-plant communities. We use maps of plants on ten dune communities around the British Isles, collected over three years,
to approach the following questions:
(a) What processes generate the seed mass/abundance
relationships reported by Rees (1995)? If they are
generated by competition-colonization trade-offs
then we predict that the relationship should be
observed at a local scale (i.e. within each site and
year), whereas if they are generated by responses to
environmental variation then the relationship
might only occur in years favourable for the recruitment of small-seeded species, and might only
emerge when data from several sites and/or years
are pooled.
(b) Do spatial arrangements of plants indicate that
competition-colonization trade-offs might structure
OIKOS 96:3 (2002)
that smaller-seeded species have more specialised
establishment requirements so would respond most
strongly to environmental variation.
Table 1. Coastal dunes upon which quadrats were established. Four sites at Holkham are distinguished by the dominant matrix-forming species.
Site
Grid ref.
Years
Aberffraw, Anglesey
Ainsdale, Mersey
Braunton Burrows, Devon
Holkham, North Norfolk
(a) Totula ruraliformis
(b) Hypnum cupressiforme var
lacunosum, Peltigera conina,
(c) Cladonia spp* (sand
deposition after first year)
(d) Cladonia spp*, Dicranum
scorparium
Kenfig, Mid-Glamorgan
Tentsmuir, Strathmore
Ynyslas, Dyfed
SH 3669
SJ2707
SS 4632
TF 8645
2
3
3
3
SS 7981
NO5127
SN 6193
Materials and methods
Site description
The precise locations of all vascular plants were
recorded within permanent quadrats that were set into
ten coastal dunes around the British Isles, four of which
were at a single site (Table 1). Fifteen annual species
within these plots were sufficiently common to be used
in spatial analyses (Table 2): nomenclature follows
Tutin et al. (1964 –80). All plots were established on
grey dunes, covered by mosses (including Dicranum
scoparium, Hypnum cupressiforme, and Tortula ruraliformis), lichens (mainly Cladonia spp), perennial
graminoids (mostly Carex arenaria, Festuca rubra, Holcus mollis, Poa pratensis), and perennial forbs. Rabbits
have a substantial impact on most of the dune systems,
grazing the stems of perennial graminoids to within a
few millimetres of the ground. It is generally agreed
that the retardation of perennials by grazing, disturbance and adverse climatic conditions allows the proliferation of annuals across the dunes (Watkinson and
Davy 1985).
In spring 1995, sets of five square quadrats (500 ×
500 mm) were demarcated with wooden stakes at each
site, being arranged in straight lines with two metres
between one another. All sites were revisited in the
springs of 1996, and seven in 1997 (Table 1). Although
sites are open to the general public, the direct impact of
trampling had little visible effect within the quadrats.
However, humans were influential in the erosion of a
weakly stabilised dune at Holkham (site b) which subsequently deposited much sand on these quadrats in
1996.
3
2
2
* included C. foliacea, C. gracilis, C. raugiformis, C. portentosa, and C. squamosa.
communities? It is not possible to identify definitively the processes that generate spatial patterns
(Pielou 1961, Lehman and Tilman 1997). One simplifying factor for us is that competition has little
effect on the seed production of the dune annuals
we investigated (Coomes et al. 2002), so competition acts primarily upon the survival of neighbours
(see Watkinson et al. 2000). If large-seeded species
were stronger competitors than smaller-seeded species, then we would anticipate that they would
increase the mortality of their neighbours and
thereby become negatively associated with other
guild members.
(c) Do the spatial arrangements of plants vary systematically with population density? We test whether
year-to-year changes in intraspecific aggregation
are related to changes in population densities. We
also test whether any emergent patterns are correlated with seed mass, because it could be argued
Table 2. Annual species found on coastal dunes (site names are abbreviated to the first two letters).
Cerastium semidecandrum†
Aira praecox
Erophila 6erna
Phleum arenarium
Myosotis ramosissima
Erodium cicutarium
Arenaria serpyllifolia
Valerianella locusta
Geranium molle
Saxifraga tridactylites
Veronica ar6ensis
Aphanes ar6ensis
Filago minima
Vulpia fasciculata
Seed mass
(mg)
Ab
Ai
Br
Ho
(a)
Ho
(b)
Ho
(c)
Ho
(d)
Ke
0.07
0.18
0.03
0.12
0.29
2.3
0.06
1.0
1.2
0.01
0.12
0.19
0.03
2.5
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
Te
*
*
Yn
*
*
*
*
*
*
*
*
*
*
† grouped with Cerastium diffusum.
OIKOS 96:3 (2002)
423
perennial vascular plants, but not the location of
mosses or lichens. In the case of rhizomatous
graminoids, the positions of ramets were recorded.
Defining and measuring aggregation, association,
and segregation
Three indices of spatial pattern were analysed, as described below (see Table 3 for a brief summary of these
indices).
Fig. 1. A schematic diagram of the mapping device used to
record the precise location of dune annuals.
The recording of plant positions
An electronic mapping device was used to record the
precise location of plants. The machine was produced
by Gnomon Survey Ltd (Marlow Bottom, Berkshire,
UK) using designs supplied by Prof. S. W. Pacala
(Princeton University, USA). As illustrated in Fig. 1,
the mapping device is held above a quadrat on a
modified tripod, and a pointing-arm (that swivels freely
on a ball-joint at the base of the mapper) is used to
point at plants within the quadrat. A system of runners
converts the arm’s angular movements into the planar
movements of a puck on a digitising pad. By this
means, the positions of plants within a quadrat are
displayed as coordinates on a computer screen. Each
quadrat is calibrated by recording the positions of the
two diagonally opposite corners (precise positioning is
aided by a laser-pen attached to the end of the arm),
and all further recordings are referenced to these. Data
were collected by pointing the arm at a given plant,
obtaining its coordinates, and then manually entering
details such as species identity and number of flowering
heads. We recorded the positions of all annuals and
Aggregation indices describe whether species are
clumped or regularly arranged. The spatial arrangement of plants is aggregated if the number of plants
observed within plant-centred circles is greater than the
number that would be expected if the pattern were
random. Consequently, the aggregation index, defined
as the observed/expected counts, would be \ 1 for
aggregated patterns and B1 for regular patterns. For
each species of annual plant at a site, we counted
conspecific neighbours within circles (of radius r)
around every plant within our five quadrats, except
plants whose circles extended outside the edges of the
quadrats. These counts were then summed to give the
observed count. An expected count was obtained by
repeating this procedure on randomised maps, in which
the positions of plants within each quadrat had been
randomised using a 2-dimensional Poisson process. A
total of 500 expected counts was obtained by re-randomising the maps using this method, from which a
distribution of expected values was obtained. The mean
was used as the denominator of the aggregation index,
while the 0.025 and 0.975 percentiles were used to
establish the 95% confidence intervals. Because the
simulations did not entail moving plants between
quadrats, the statistics provide a measure of withinquadrat aggregation. In other words, if the numbers of
plants in each quadrat differed markedly, but plants
were randomly arranged within any one quadrat, our
methods would signify that the patterns were indistinguishable from random. We counted neighbours within
circles of radius 10, 30 and 50 mm to provide aggregated indices at three scales.
Table 3. Methods for calculating the observed and expected values for three indices of spatial pattern (each defined as
observed/expected), based on standard methods (Ripley 1981, Upton and Fingleton 1985, Cressie 1991).
Index
Observed values
Expected values (repeated for 500 simulations)
Aggregation
Count number of conspecific neighbours within a
circle around each plant
Count number of neighbours of species j within a
circle around each plant of species i
Randomise positions of plants using a Poisson
process. Count number of conspecific neighbours
Randomise the position of species i relative to j,
while maintaining the intraspecific patterns. Count
number of neighbours of j around i
Random shuffle the identity of each plant while
maintaining the spatial patterns. Calculate the odds
ratio
Association
Segregation
424
Odds ratio of having a conspecific rather than a
heterospecific nearest neighbour
OIKOS 96:3 (2002)
Association indices. Two species are said to be negatively
associated if the number of plants of one species within
circles centred around the second species is less than
would be expected within randomly positioned circles.
Similarly, species are positively associated if there is a
surplus (rather than deficit) of heterospecific neighbours.
An association index (SI), defined as the observed/expected numbers of heterospecific neighbours around a
target species, is \1 for positive associations and B 1
for negative associations. The association between species does not depend upon whether the intraspecific
pattern of either species is random, clumped or regular,
but the variance of the null distribution depends greatly
on the intraspecific patterns.
For each species of annual plant at a site, we counted
heterospecific neighbours within circles of radius r
around all plants of the focal species, except plants
whose circles extended outside the edges of the quadrats.
The counts were summed to give the observed numbers
of neighbours. An expected count was obtained by
repeating this procedure on randomised plant maps,
which were generated by randomising the position of
one species relative to the others within each quadrat,
while maintaining their intraspecific spatial characteristics. This was achieved by randomising the positions of
cluster centres identified by the clump-recognition process (Coomes et al. 1999), an alternative to the toroidal
shift approach (Upton and Fingleton 1985). The mean
count obtained from 500 such simulations was used as
the denominator of the association index, and the 0.025
and 0.975 percentiles of the distribution gave the 95%
confidence intervals.
Previous studies have described pairwise associations
between species using complex matrices or figures
(Mahdi and Law 1987). While this approach is useful in
emphasising the disparity between the ‘plant’s-eye’ and
the ‘mean-field’ views of the competitive environment,
we feel that the inclusion of such details would cloud
rather than clarify our arguments, not least because we
have 27 such matrices, each containing 3 – 10 annual
species and 2 –10 perennials, producing over 135 measures of aggregation and 20 000 measures of association.
The presentation of results was simplified after extensive
analyses showed that the vast majority of pairwise
associations were non-significant ( \95%). Therefore,
we decided to test the association between each annual
species and the following groups: (a) other guild members, (b) perennial graminoids, (c) perennial forbs, and
(d) Galium 6erum and Sedum acre. Group (d) was
distinguished from the other perennial forbs because
these species are commonly found in sites of fresh sand
deposition.
Segregation indices. Two species are defined as segregated when there is a greater probability of having a
conspecific nearest neighbour than expected by chance
(which is influenced by both the degree of aggregation
OIKOS 96:3 (2002)
and association). Segregation occurs as a result of
intraspecific aggregation and/or negative associations
between species. We use Dixon’s index of segregation:
SAA = ln
n
NAA /NAB
,
(NA − 1)/NB
where NA and NB are the number of plants of species A
and B, respectively, and NAB is the number of plants of
species A with species B as their nearest neighbour
(Dixon 1994). Values of SAA \ 0 indicate that species are
segregated. This particular index is based on the identity
of nearest neighbours, and not upon the distances
between plants: it does not have a scale component. We
measured the degree of segregation between each annual
species and the groups outlined in the previous section.
A segregation index was estimated in each of the five
quadrats at a site, and t-tests were used to test whether
they differed significantly from zero.
Statistical tests of variation between sites, years
and species
The influences of species, site, and year on aggregation
and association indices were analysed by generalised
linear modelling (Aitkin et al. 1989). The models we used
are given in the Appendix and referenced within the text
using numerical superscripts. The overall distributions of
aggregation and association indices were approximately
log-normal, so analyses were performed with log-link
functions. The scaling of the variance with respect to
mean was selected using quasi-likelihood methods, such
that plots of the Pearson’s residuals showed no trend.
This approach ensured that statistical tests were conservative even when over-dispersion occurred.
Results
Population structure
The number of annuals at the ten sites fluctuated greatly
between years (Fig. 2). Eight of the ten sites had fewer
plants in 1996 than in 1995, with loge[Nt + 1/Nt ] averaging −0.366 (SEM = 0.14, t9 = − 2.4, P=0.03)1. Furthermore, the increased number of annuals at one site
can be attributed to winter storms that transformed a
closed lichen bed with few annuals into an open sandy
area (Holkham site ‘b’). The numbers of annuals neither
increased nor decreased consistently among the sites
between 1996 and 1997: they increased at five sites and
declined in two sites, with log[N1997/N1996] averaging
0.049 (SEM 0.11, t6 = 0.45, P =0.69)1.
A previous paper found consistent negative relationships between seed mass and abundance on coastal
dunes around the British Isles (Rees 1995). When we
425
Fig. 2. Changes in the population densities of dune annuals at
ten locations over three years.
analysed our data using a similar method to that of
Rees (1995), pooling data across sites and years, we
also found a highly significant overall relationship
(F1,152 =7.7, PB 0.001)2 (Fig. 3). In contrast when we
Fig. 4. Intraspecific aggregation within circles of 10, 30 and 50
mm radius. Indices greater than one indicate aggregation. The
means and standard errors were estimated by pooling indices
from all species at all sites and years.
conducted more conservative tests, for relationships at
each site and in each year, we found no significant
relationships in 1995 (F10,48 = 1.02, P\0.20)3, 1996
(F10,45 = 0.49, P\ 0.20)3, or 1997 (F7,30 = 1.55, P\
0.20)3. Neither were the population growth rates of
species, log(Ni,Y + 1/Ni,Y ), related to their seed mass,
either in 1996/1995 (F10,45 = 1.1, P\ 0.2) or in 1997/
1996 (F7,30 = 1.2, P\ 0.2)4.
Aggregation
Fig. 3. Relationship between seed mass and abundance of
dune annual species, pooling data from all sites and years
(F1,152 = 7.7, PB 0.001). More conservative tests at each site in
each year found no statistically significant relationships. Note
that statistical analyses were performed on log-log transformed
data, but the figure shows non-transformed data to enable
comparisons with Rees (1995).
426
Most species were significantly aggregated at most sites
and in most years: 79% and 91% of aggregation indices
were significant at the 10-mm and 50-mm scales, respectively (P= 0.025). Nearly all of the patterns (94%) were
more aggregated at the 10-mm than at the 50-mm scale.
The average individual had 3.5 times as many conspecific neighbours within a 10-mm radius than expected
by chance, and 1.8 times as many neighbours within 50
mm (Fig. 4). The degree of aggregation was not significantly related to seed mass at any of the scales considered (P\ 0.1 for all comparison)5.
Generally, species became more aggregated (at the
50-mm scale) in years when they were relatively uncommon (Fig. 5): such relationships were found at eight of
the ten sites (F10,56 = 6.7, P= 0.001)6. Within this
OIKOS 96:3 (2002)
Fig. 5. Consequences of year-to-year population fluctuations
on the spatial aggregation of species. Population fluctuations
are shown as changes in population size from 1995 to 1996,
and 1996 to 1997, while changes in spatial aggregation are
shown as the ratio of aggregation indices in these consecutive
years (r =50 mm). In years when species become rare, they
also become more spatially aggregated (1995/96 r = −0.597,
P B 0.01; 1996/97 r= −0.68, PB0.01).
framework we found that small-seeded species became
highly aggregated when rare, while larger-seeded species
were less affected (r= 0.68, P=0.05, Fig. 6). The slopes
of the relationships between abundance and aggregation (50-mm scale) were significantly negative (at PB
0.05) for five of the seven smallest-seeded species (Aira,
Cerastium, Erophila, Saxifraga, and Veronica), non-significantly negative (P\ 0.10) for three species mostly
with intermediate seed mass (Arenaria, Myosotis, and
Phleum), and non-significantly positive (P\ 0.10) for
Fig. 6. The relationship between seed mass and the extent to
which species becomes spatially aggregated in years when they
are rare (r =0.68, P=0.05). The slopes of the abundanceaggregation relationships were found by regressions of
log(NY + 1/NY ) against log(AIY + 1/AIY ) for each of the species
found at more than one location (species acronyms are St =
Saxifraga tridactylites and so forth). Five of these slopes
significantly differed from zero (filled circles).
OIKOS 96:3 (2002)
Fig. 7. Degree of aggregation of species, calculated as
log(AI(30)), in relation to their relative abundance at a particular site in a given year. Rarer species tend to be more
aggregated (sites differences are not shown here, but were
included in statistical analyses).
the two largest-seeded species (Erodium and
Valerianella).
The negative relationship between population size
and aggregation (50-mm scale) was not confined to
within-species comparisons over time, but was also
observed for among-species comparisons within sites
(F27,70 = 4.1, P =0.0001)7 (Fig. 7). All but one of the 27
relationships between Nt and AI(50) had negative
slopes, and these were significantly negative in five sites
(i.e. significant for one or more years).
Associations
Annual plants tended to be positively associated with
other annuals at all scales (Fig. 8a). At the 50-mm
scale, 41% of associations tested were significantly positive. The most likely explanation for these positive
associations is that patches within the quadrats are
inhospitable to all annual species, so the remaining
areas contain more plants than expected. Erodium or
Geranium were the only species observed to have significant negative associations with other annuals (at the
10-mm scale), almost certainly because these largeseeded species form basal rosettes of leaves that are
capable of killing nearby plants (Fig. 8).
We hypothesized that large-seeded species would be
negatively associated with other guild members if competition was important. Tests showed that there were
significant relationships between seed mass and degree
of association at the 10-mm scale (F27,75 = 2.33, PB
0.0001)8. Examination of the slopes of these relationships (by site and year) showed that the majority were
negative (19 of 27), but that few were statistically
significant (4 of 27). In the first year, when populations
427
were relatively large, the relationships tended to negative, suggesting that competitively induced mortality
was one of the processes structuring the community
(Fig. 9). In the second year, when many populations
had crashed, the relationships were close to zero or
positive, suggesting that establishment and survival had
more importance than competitively induced mortality
in defining the pattern. No clear patterns emerged in
the third year (Fig. 9).
The vast majority of association tests between annuals and dicotyledonous perennials or graminoids were
non-significant at the 50-mm scale (Table 4). However,
most of the significant associations were found to be
positive (11%), and were particularly common for association with Sedum acre and Galium 6erum – these
species had been singled out because they are commonly associated with disturbed sites, so it did not
come as a surprise to find positive associations between
annuals and these species (Table 4).
Segregation
Dixon’s segregation indices suggested that annuals were
segregated from guild-members (i.e. SAA \ 0) in 98% of
comparisons, of which 43% were significant. These
results reflect the fact that intraspecific aggregation was
generally stronger than the counteracting effects of
positive association among annuals. Unsurprisingly,
species that tended to be highly aggregated also had
Fig. 8. Associations (with
standard errors) between
annual species and (a) other
guild members, (b)
perennial graminoids, (c)
perennials dicotyledonous,
and (d) Sedum acre and
Galium 6erum. Association
indices greater than one
indicate positive
associations, while values
less than one indicate
negative associations.
428
OIKOS 96:3 (2002)
British coastline, and in three of the four habitats at
Holkham, and causing an average decline in plant
number from 1900 m − 2 in 1995 to 900 m − 2 in 1996.
The synchrony of the population crash across disparate
sites points to the influence of some aspect of the
weather conditions, quite possibly a spring drought
such as the one which caused massive mortality of
Cerastium semidecandrum at Holkham in 1985 (see Fig.
1 of Rees et al. 1996). The argument that cyclic or
chaotic dynamics could have produced these results
cannot be totally dismissed but seems highly unlikely,
given that the population crashes were synchronised
over a large scale, and that density-dependent models
indicate that annuals tend to have highly stable dynamics in the absence of between-year climatic variation
(Watkinson 1980, Rees and Crawley 1989, Rees et al.
1996, Watkinson et al. 2000).
Perhaps our most striking finding was the extent to
which species became aggregated when rare: this result
was found by examining intraspecific changes in pattern
over time, and interspecific patterns across dunes. Similar findings have been documented for invertebrate
animals (Hassell 1980, Hassell et al. 1987, Davis and
Pedigo 1989), but not to our knowledge for plants. The
shifts in pattern may reflect that ‘bad’ weather renders
patches of dune inhospitable in some years, restricting
annuals to refuges, while ‘favourable’ weather allows
the species to again establish over wider areas. Refuges
could play an important role in promoting species
coexistence. Our results are consistent with the finding
of Watkinson et al. (2000), who showed that extinction
of Vulpia ciliata within small patches of dune (ca
20× 20 cm) was an important component of this species’ dynamics, but that patches are rapidly recolonized
from neighbouring areas. Intraspecific aggregation can
lead to reduced contact with other species, shifting the
balance of inter- to intra-specific competition in favour
of coexistence (Pacala 1986, Rees et al. 1996). We
hypothesize that increased aggregation of rare plants
may thereby decrease the chances of their extinction;
Fig. 9. Relationship between species association with other
guild members – calculated as log(SI(10)) – and seed mass in
(a) 1995, (b) 1996, and (c) 1997.
high indices of segregation (e.g. SAA Saxifraga 0.39,
Valerianella 0.32 at Holkham). The strength of segregation was unrelated to seed mass (F27,75 =1.66, P=
0.24)9.
Table 4. Numbers of significant positive (+), negative (−),
and non-significant (NS) associations between each annual
species and other groups of species (P =0.01), at the 10-mm
and 50-mm scales. Associations were tested by 500 Monte
Carlo simulations in which the patterns of each species were
randomised with respect to one another while retaining their
marginal properties.
Associations with
r (mm)
+
−
NS
Other annuals
10
50
10
50
10
50
10
50
22
48
1
7
1
11
7
19
2
3
3
3
2
2
2
1
93
65
111
106
112
103
85
74
Discussion
Graminoids
Seed mass and year-to-year environmental
variation
Dicot perennials
The 1996 crash in the population of annuals was consistent, occurring at six of the seven sites around the
OIKOS 96:3 (2002)
Sedum and Galium
429
this is potentially an important mechanism by which
the risk of local extinct of rare species is reduced.
The observation that small-seeded annuals become
more aggregated in times of relative rarity than largeseeded species (Fig. 6) supports a growing literature
demonstrating that small-seeded species are more likely
to die as seedlings from desiccation (and other factors),
and have more specialised regeneration requirements
(Watkinson 1981, Mazer 1989, Leishman and Westoby
1994, Crawley and Nachapong 1985, Burke and Grime
1996, Metcalfe et al. 1998). Thus, seed mass may regulate species responses to year-to-year environmental
variation.
Seed mass and the competition-colonization
trade-off
Our data do not support the view that the competitioncolonization trade-off is consistently important in defining the dynamics of annual plants, although it may
contribute to dynamics in years when population sizes
peak. We found significant negative associations between the two largest species and the rest of the guild
(at the 10-mm scale), almost certainly indicating local
exclusion of smaller-seeded species through competition, but only in 1995 when population densities were
high.
Rees (1995) used the observation that smaller-seeded
species tended to be more abundant on coastal dunes to
support his hypothesis that the dynamics of dune-annual communities are driven by competition-colonization trade-offs. We also found a negative relationship
between seed mass and abundance, but only when
analysing our data using a similar approach to that of
Rees (1995) – pooling data across years and sites (Fig.
4) – and not when we examined the relationships at
any specific site and year. Our analyses suggest that
differential responses to environmental variation produced the seed mass/abundance relationship, for reasons outlined in the introduction, although we cannot
entirely dismiss the role of the competition-colonization
trade-off, as the statistical power of tests within-site and
year comparisons were relatively weak.
We believe that the competition-colonization tradeoff needs to be placed in the context of other processes
affecting dune communities. Since the dune annuals are
spatially segregated from one another, and large-seeded
species tend to be rare, the frequency of competitive
interactions between large- and small-seeded species is
often low, so the trade-off may not exert a major
influence on dynamics in the majority of years. Furthermore it may not be the case that large-seeded species
are strongly competitive under the nutrient poor and
often droughted conditions found on dunes; even
though several experiment show large-seeded species
tend to outcompete smaller-seeded when annuals are
430
grown in glasshouses with plenty of water (see Rees
1995 for references). Our pattern analysis suggests that
competition may contribute towards the dynamics of
dune communities in some years, while climatic influences are more pervasive in others. These results agree
with a seed-sowing experiment we conducted on the
Holkham dunes, which showed clear density-dependent
effects during the ‘good’ year of 1997, but no competitive effects for the ‘bad’ year of 1996 (Coomes et al.
unpubl.).
We argue that not only competitive processes, but
also colonization processes vary tremendously from
year to year. In particular the relationship between a
species’ fecundity and survivorship is likely to respond
strongly to climatic variability (Mack and Pyke 1984,
Kelly 1989). For example, Turnbull et al. (1999)
demonstrated that small-seeded annuals in limestone
grassland tended to produce far more seeds than largeseeded species, but are also much more likely to die
before reaching maturity. Although a component of
this mortality is likely to result from competitive processes, it is very likely that much is independent of
density (Watkinson 1981; cf. Watkinson et al. 2000).
Whether or not populations show positive growth rates
is likely to hinge on the fecundity-survival relationship.
For example, Turnbull et al. (1999) sowed seeds at the
start of what proved to be a very bad season for the
annuals, with seed production averaging only 0.9% of
that in the previous year (range among species 0.1 –
3.7%). The only species to have population growth
rates greater than one were tiny-seeded, while the larger
seeded species all had near-zero population growth
rates, despite evidence of their competitive superiority.
Other possible influences of seed mass
The dynamics of dune annuals also need to be put in
the context of successional processes: there is a continual process of fresh sand deposition, followed by stabilised sand enriched with organic matter, leading
eventually to domination by lichens (Salisbury 1952).
The species within the annual-plant guild had similar
habitat requirements at any one site (Janssen 1973),
resulting in the positive associations observed, so our
data do not support the hypothesis that species are
differentiated according to micro-habitat preferences
(cf. Bonis et al. 1997, Turnbull 1997). On the other
hand, differences in species composition among sites
(e.g. the four contrasting habitats at Holkham) may
well reflect niche specialisation along a successional axis
(Pemadasa et al. 1974): at least some large-seeded species are restricted to the later successional, more nutrient rich sites (Valerianella locusta, Veronica ar6ensis
and Vicia lathyroides), while in Eastern England some
of the tiniest-seeded species (e.g. Saxifraga tridactylites)
are restricted mainly to winter-wet hollows.
OIKOS 96:3 (2002)
Does seed mass influence community structure?
Our data support the view that a seed-mass regulated
competition-colonization trade-off might be important
in some years. We have also shown that seed mass is
likely to be influential in other processes, such as responses to year-to-year variation in environment, and
possibly niche differentiation along successional gradients. However, we recognise that factors unrelated to
seed size may play an important role in community
dynamics. For example, annual species were spatially
segregated from other guild members in 98% of the
tests we made, but the degree of segregation was unrelated to seed size. This spatial segregation may profoundly alter competitive interactions, as argued by
Rees et al. (1996) and Pacala and Levin (1997). We
recommended that more research effort is put into
defining the influences of seed mass, particularly the
temporal variability in fecundity-survival relationships.
Seed-sowing experiments conducted over several years
would be helpful in furthering this debate.
Acknowledgements – DAC was supported by a NERC postdoctoral research grant. We thank Steve Pacala for providing
the designs from which the mapping device was made, and for
insightful conversations about spatial processes. Karel Alders
and Glyn Jones spent many bitterly cold spring days lying on
dunes mapping plants. Risto Virtanen kindly identified the
lichens and mosses. We thank the wardens of the coastal dunes
for their support, and the Earl of Leicester for granting access
to the Holkham dunes. Richard Duncan provided helpful
comments on the manuscript.
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Appendix
Statistical analyses, labelled in the text by numerical superscripts, were performed by comparing the deviances of nested generalised
linear models (Aitkin et al. 1989). The following response variables were used for a given species at a given site in year Y: (a)
NY =number of plants, (b) AIY = aggregation index, (c) SIY =association index, and (d) SSY =association index. Factors in the
models were Year (1995, 1996, 1997) and Site (ten in 1995 and 1996, seven in 1997), while covariates were seed mass (SM), and
population size NY. The sign ‘:’ means an interaction term. Not all species are represented at all sites (Table 1).
1*
2
3†
4‡
5
6‡
7
8
9
Model
Simplified model
log(S NY+1/S NY )= c
log(NY )log(SM)+site+year
log(NY )= site: log(SM)+site
log(NY+1/NY )= site: log(SM)+site
log(AIY )= site:year: log(SM)+site:year
log(AIY+1/AIY )= site: log(NY+1/NY )+site
log(AIY )= site:year: log(NY )+site:year
log(SIY )= site:year: log(SM)+site:year
log(SSY )= site:year: log(SM)+site:year
log(NY )site+year
log(NY ) =site
log(NY+1/NY ) =site
log(AIY ) =site:year
log(AIY+1/AIY ) =site
log(AIY) =site:year
log(SIY ) =site:year
log(SSY ) =site:year
* Total number of plants of annual species at each site. Student’s t-test with null hypothesis c =0.
† Separate tests for each year.
‡ Separate tests for 1995/96 and 1996/97.
432
OIKOS 96:3 (2002)