Download Trait-dependent modification of facilitation on cobble

Ecology, 90(11), 2009, pp. 3042–3050
Ó 2009 by the Ecological Society of America
Trait-dependent modification of facilitation on cobble beaches
ANDREW D. IRVING1
AND
MARK D. BERTNESS
Department of Ecology and Evolutionary Biology, Brown University, Box G-W, Providence, Rhode Island 02906 USA
Abstract. Fundamental gaps remain in our knowledge of how positive species
interactions, such as facilitation and mutualism, structure and maintain populations and
communities. Foundation species create extensive biogenic habitats, but we know little of how
their traits, such as density, age, and patch size, modify their ability to facilitate other species.
We tested the role of facilitator traits in cobble beach plant communities in New England,
USA. In this system, intertidal beds of the cordgrass Spartina alterniflora facilitate populations
of halophytic forbs at higher shore elevations by buffering wave action, stabilizing cobbles,
and limiting physical disturbance. Using descriptive and experimental techniques, we tested
the hypotheses that (1) the density and height of cordgrass shoots modify the strength of the
cordgrass–forb facilitation, and (2) cordgrass peat alone contributes to the facilitation of
forbs. Increased shoot density, as well as the combination of cordgrass peat and shoots,
positively affected two life history stages (seedling and adult) of the abundant forb Suaeda
linearis, demonstrating that cordgrass traits modify the strength of facilitation in this system.
Since the expression of traits varies within and among patches of any given foundation species,
traits can and should be used to predict the strength of facilitation, to guide the development
of conservation strategies, and to develop more accurate models of species interactions.
Key words: cobble beach; facilitation; foundation species; habitat; Spartina alterniflora; species
interaction; Suaeda linearis.
INTRODUCTION
Species interactions are central for shaping patterns of
distribution and abundance, and to theories of community dynamics (e.g., Paine 1980, Menge and Sutherland
1987, Tilman 1994). Interactions range from negative to
positive, but ecologists have historically focused on
negative interactions, such as competition and predation, as key structuring forces (Hairston et al. 1960,
Tilman 1982, Keddy 2001). Positive species interactions,
such as facilitation and mutualism, have long been
recognized (Clements 1916), but their role in shaping
communities has only recently been appreciated (see
reviews by Bertness and Callaway 1994, Callaway 1995,
Stachowicz 2001, Bruno et al. 2003). Notable theoretical
cornerstones, including niche theory, the intermediate
disturbance hypothesis, and environmental stress gradients, require substantial rethinking when positive
interactions are considered (Bruno et al. 2003).
Facilitation through biogenic habitat provision is a
widespread type of positive interaction. By growing and
completing their life cycle, foundation species (sensu
Dayton 1972) such as trees, shrubs, salt marsh grasses,
corals, kelps, seagrasses, and mussels, create extensive
Manuscript received 21 October 2008; revised 6 January
2009; accepted 17 February 2009. Corresponding Editor: D. A.
Spiller.
1 Present address: South Australian Research and Development Institute (Aquatic Sciences), P.O. Box 120, Henley
Beach, South Australia 5022 Australia.
E-mail: [email protected]
habitats that enhance the fitness and distribution of
other species directly, by providing living space and food
resources, and indirectly, by providing refuge from
predators and abiotic stress (Jones et al. 1994, Bruno
and Bertness 2001, Grutter and Irving 2007). The
subsequent ensembles of negative and positive interactions among facilitated species (Altieri et al. 2007)
cumulatively affect emergent ecosystem properties such
as productivity, nutrient cycling, and diversity (Stachowicz 2001).
While facilitation by most foundation species is
recognized, we know little of how their individual- and
population-level traits modify the strength of facilitation
(i.e., the amount by which environmental conditions are
modified and other taxa are facilitated; Bruno and
Bertness 2001). Trait variation can change the amount
of habitable space, resource availability, and amelioration of environmental stress (Gleason et al. 1979,
Leonard and Luther 1995), and may therefore substantially modify the strength of facilitation. For example,
population-level traits such as plant density, aboveground biomass, and patch orientation to prevailing
currents can all modify the ability of seagrass beds to
facilitate fish and invertebrates (Heck and Wetstone
1977, Fonseca et al. 1996, Tanner 2003), while long-term
declines in fish abundance and diversity occur when
coral biomass and complexity are reduced (Syms and
Jones 2000). In terrestrial environments, the individuallevel trait of a plant’s canopy architecture can influence
the degree of environmental modification (e.g., shading)
and therefore modify its potential as a nurse plant
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TRAIT-DEPENDENT FACILITATION
(Drezner 2006). Overall, however, rigorous experimental
evidence of the role of facilitator traits is lacking for
most systems (Bruno and Bertness 2001). Such knowledge would nevertheless be useful for developing
facilitation theory, predicting community structure
under altered environmental conditions, and for identifying conservation priorities.
The purpose of this study was to address this
knowledge gap in a system where underlying facilitative
mechanisms are understood. On cobble beaches in New
England, USA, the cordgrass Spartina alterniflora forms
extensive intertidal beds of dense peat and seasonal
aboveground shoots (April–October) that create habitat
for marine mussels, barnacles, gastropods, amphipods,
crabs, and algae (Altieri et al. 2007). Beds longer than
;25 m also facilitate communities of annual and
perennial halophytic forbs higher on the shore by
buffering wave energy, stabilizing cobbles, and limiting
burial and disturbance at critical early life history stages
of forb seedling emergence and establishment (Bruno
2000, Bruno and Kennedy 2000; see Plate 1 and
Appendix A). In the absence of cordgrass, or when
beds are shorter than 25 m, forbs germinate but even the
most tolerant species are unable to establish because of
physical disturbance from unstable cobbles (Bruno
2000, Bruno and Kennedy 2000).
The dependence of forbs on cordgrass beds greater
than 25 m in length already demonstrates a traitdependent threshold for facilitation (i.e., patch size:
Bruno and Kennedy 2000), yet within and among these
larger beds, other population-level traits such as
cordgrass shoot density and height can vary greatly.
Variation of these traits alters hydrodynamics and
sediment accretion within cordgrass beds (Gleason et
al. 1979, Leonard and Luther 1995), making it possible
that the facilitation of forbs is also affected, given their
reliance on the reduction of wave energy by cordgrass
(Bruno 2000). To explore this question, we correlatively
examined the relationship of forb abundance with
cordgrass shoot density and height, and then experimentally manipulated shoot density and height to test
the hypothesis that these two population-level traits
modify cordgrass facilitation of forbs (survival and per
capita biomass).
In addition to cordgrass shoots, the peat base may
contribute to forb facilitation because it can form a
distinct wall up to ;1 m tall that buffers wave energy
and stabilizes cobbles (A. Irving and M. Bertness,
personal observations). The peat base mostly comprises
compacted layers of dead cordgrass shoots and roots
that slowly accrete over time, and within which the short
shallow roots of living cordgrass can anchor. Living
cordgrass root biomass forms a relatively minor
component of peat, so while the peat is an integral part
of the entire cordgrass bed, it could be considered a
distinct structural element in the context of the
cordgrass–forb facilitation. Indeed, an earlier experiment that removed cordgrass shoots (i.e., leaving only
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peat) found that water flow and cobble instability
increased relative to areas where cordgrass remained
intact, but were still below levels observed in the absence
of cordgrass beds (termed ‘‘interbed’’ habitats; Bruno
and Kennedy 2000). Even so, the relative contribution of
peat to the cordgrass–forb facilitation is unknown, so
the hypothesis that cordgrass peat contributes to the
facilitation of cobble beach forbs was tested by
experimentally removing shoots (leaving peat) and
comparing forb survival and per capita biomass to
those behind intact shoots and to those in interbed
habitats.
MATERIALS
AND
METHODS
Study sites
Research was done on intertidal cobble beaches of
Narragansett Bay in Rhode Island, USA, a well-mixed
estuary with semidiurnal tides ranging between 0.8–2 m.
Two sites were used; Providence Point on Prudence
Island (41840 0 N, 71820 0 W) and Haffenreffer Reserve
(hereafter called Haffenreffer, 41841 0 N, 71814 0 W). Both
sites support extensive cordgrass beds and abundant
forb populations (Bruno 2000, Bruno and Kennedy
2000, Kennedy and Bruno 2000).
Does shoot density and height modify cordgrass
facilitation of forbs?
Testing the hypothesis that forb abundance correlates
with cordgrass shoot density and height was done in late
June 2006 when cordgrass had completed much of its
seasonal growth. At each site, the density and height of
cordgrass shoots within 2 m of the upper margin of beds
were sampled with haphazardly placed quadrats (0.2 3
0.2 m, n ¼ 40 for density and an independent 40 for
height). Forbs adjacent to each sampled patch of
cordgrass (0.5–2 m away from the upper border) were
then counted using larger quadrats (0.5 3 0.5 m) because
of their lower densities and less uniform distribution
relative to cordgrass (all values were converted to
density/m2 for analyses). Linear regression of untransformed data was used to examine the relationship of
forb abundance with shoot density and height.
To experimentally test the hypothesis that cordgrass
shoot density and height modify forb facilitation, shoot
density within 10 patches of cordgrass was halved by
manual thinning (termed ‘‘sparse,’’ ;250 shoots/m2),
while another 10 patches were left at natural densities
(‘‘dense,’’ ;530 shoots/m2). Thinning cordgrass involved
the ‘‘weeding out’’ of individual shoots and associated
short roots, but rarely any attached peat, and was done
evenly from the upper to lower border of the cordgrass
bed and across a width of ;2 m (total area thinned
;10–16 m2 per replicate), leaving unmanipulated
cordgrass on either side. Shoots in five patches of each
density treatment were then trimmed with shears to
about half their natural height (‘‘short,’’ ;30–40 cm),
while the remaining patches in each density treatment
were undisturbed (‘‘tall,’’ ;75–90 cm; experimental
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ANDREW D. IRVING AND MARK D. BERTNESS
Ecology, Vol. 90, No. 11
design, 2 density 3 2 height 3 5 replicates). Treatments
were established only at Providence Point due to space
restrictions at Haffenreffer, and were maintained every
two weeks. Immediately behind each replicate, permanent quadrats (1 m2) were marked and the abundance of
forbs within was quantified on haphazardly chosen days
throughout the growing season.
Multiple species of forb were present but only one,
Suaeda linearis (family Chenopodiaceae, commonly
known as sea-blite), consistently occurred in great
enough abundance for meaningful experimentation
and analysis. Given the reliance of the entire forb
community on the presence of cordgrass (Bruno 2000),
other species may have shown similar responses to our
experimental manipulations, but their abundances were
too low to draw such conclusions with confidence.
Experiments initially focused on S. linearis seedlings
because their facilitation by cordgrass is the proximate
life history stage limiting forb population size and
distribution (Bruno 2000). However, most forbs in this
system are annuals that depend on seed supply from
prior seasons to maintain populations, and so experiments were repeated with adult S. linearis (using an
independent set of cordgrass manipulations) and focused on survival and seed production. Experiments
using seedlings began on 4 May and finished on 15 June
(42 days), when S. linearis began a period of rapid
growth into adults ( personal observations). Experiments
using adults began on 21 June and finished on 4
September (75 days) when seeds were present and early
signs of senescence were visible (e.g., withering of
leaves).
The percentage survival of S. linearis was calculated
as the proportion of final to initial abundance, with
analyses of arcsine-transformed data following two-way
ANOVA and treating density and height as fixed and
orthogonal factors. In addition, five individuals (representing 1–22% of the population of forbs in each
replicate across treatments) were haphazardly sampled
from each quadrat to quantify per capita biomass and
seed production. Biomass was quantified by removing
belowground tissue and oven drying plants to a constant
mass (708C for 48 hours), while seed production per
plant was estimated by multiplying the number of seeds
present on a representative branch from each plant by
the number of branches with seeds. For these variables,
the mean value of the five individuals per quadrat was
used as a single replicate for statistical analyses,
following assumptions of independence for ANOVA.
While the results of these formal analyses are shown
herein, alternate P values derived from BonferroniHolm adjustments are shown in Appendix B for
comparisons.
season to create clearances ;2 m wide from the upper to
lower margin of the bed (n ¼ 5 clearances per site).
Shoots were cut to a height of 1–3 cm using a garden line
trimmer, with loose plant material removed after each
cutting. The response of S. linearis in this clearance
treatment (termed ‘‘peat only’’) was compared to uncut
cordgrass (‘‘shoots and peat’’) as well as to nearby
‘‘interbed’’ habitats at equivalent tidal heights. The
experiment was repeated for S. linearis seedlings (May–
June) and adults (June–Sept.), with survival, biomass,
and seed production quantified as described above.
Analyses were done with one-way ANOVA, with
survival data arcsine transformed (Bonferroni-Holm
adjustments also shown in Appendix B).
It is worth noting that while peat is certainly an
integral component of cordgrass beds, we only tested the
contribution of peat to the facilitation of forbs and not
the role of variation in traits of peat (e.g., peat height or
width) given the enormous logistical difficulties in
creating such treatments. Also, the experimental clearance of shoots did not appear to affect cordgrass root
biomass anchored within the peat because regrowth of
shoots was rapid and constant, requiring the maintenance of treatments (removal of new shoot growth) on a
weekly basis. As such, the ‘‘peat only’’ treatment can be
considered a combination of primarily dead (peat) and
living (roots) cordgrass biomass.
Does peat facilitate forb success?
Does shoot density and height modify cordgrass
facilitation of forbs?
To experimentally test the hypothesis that cordgrass
peat contributes to the facilitation of forbs, cordgrass
shoots were removed weekly throughout the growing
Water flow and cobble stability measurements
Since facilitation of forbs by cordgrass occurs through
cordgrass buffering water flow and stabilizing cobbles,
these variables were quantified in each experiment.
Water flow was estimated from the dissolution of plaster
blocks (Yund et al. 1991). Five replicate blocks were
secured with epoxy on the surface of large stable cobbles
in each treatment, ;0.5 m behind the upper margin of
cordgrass (equivalent height for interbed treatments),
and left for 9–12 days. Blocks were oven dried (708C for
48 hours) before and after deployment, with change in
mass used to calculate the percentage dissolved per day.
Cobble stability was quantified using the method of
Bruno and Kennedy (2000). Small cobbles of similar size
(;4 cm diameter) and shape (approximately round)
were collected from study sites. In each experimental
replicate, five individually numbered cobbles were
placed at regular distances on a transect ;0.5 m above
the upper margin of cordgrass. These cobbles were
located the following day (after two tidal cycles) and the
linear distance each had moved was measured. The
mean distance of the five cobbles within each replicate
was used as a single replicate for statistical analyses.
RESULTS
Forb abundance correlated positively with cordgrass
shoot density and height (Fig. 1a, b). Similar relation-
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FIG. 1. Correlations of forb abundance (all species combined) with (a) cordgrass shoot density and (b) cordgrass shoot
height. Both sites were pooled since similar trends were
observed.
ships were observed between sites, so data were
combined for final analysis. Variation in shoot density
explained 44% of the intrabed variation in forb
abundance, while shoot height explained 29%.
TABLE 1. Results of two-way ANOVAs testing the effects of
cordgrass shoot density (dense vs. sparse) and height (tall vs.
short) on the survival of S. linearis seedlings and adults.
Stage and source
df
MS
F
P
Seedling
density
height
density 3 height
residual
1
1
1
16
8149.80
2252.27
1051.74
167.96
48.54
13.41
6.26
,0.0001
0.0021
0.0235
Adult
density
height
density 3 height
residual
1
1
1
16
6026.87
318.87
6.09
301.76
19.97
1.06
0.02
0.0004
0.3193
0.8888
Notes: Significant results are shown in boldface type. The
data analyzed are for the final day of sampling. All data were
arcsine transformed prior to analysis. Cochran’s C test of
homogeneity of variances: P . 0.05 for each test.
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FIG. 2. Effects of cordgrass shoot density (dense vs. sparse)
and height (tall vs. short) on the mean (6SE) percentage
survival of S. linearis (a) seedlings, and (b) adults. Note that
survival may exceed 100% as more S. linearis emerged after the
experiment was established. Day 1 for seedling experiments was
4 May; adult experiments began on 21 June.
Manipulating cordgrass shoot density and height
significantly affected S. linearis survival (Table 1). Dense
cordgrass maintained seedling survival at ;100%, while
sparse cordgrass reduced survival to ;76% when tall, or
;40% when short (Fig. 2a; Table 1, density 3 height
interaction; SNK tests, dense and tall ¼ dense and short
. sparse and tall . sparse and short). Survival of adults
was ;35% greater behind dense cordgrass, and was
unaffected by height manipulations (Fig. 2b; Table 1,
density main effect; SNK tests, dense . sparse).
Thinning cordgrass also reduced seedling and adult
biomass by up to 82% and 63% respectively (Fig. 3a, b;
ANOVA density main effect, F1,16 ¼ 27.31, P ¼ 0.0001
for seedling biomass, F1,16 ¼ 7.28, P ¼ 0.0158 for adult
biomass), and reduced seed production by as much as
57% (Fig. 3c; ANOVA density main effect, F1,16 ¼ 4.70,
P ¼ 0.0455). Manipulating cordgrass height only
affected seedlings behind sparse cordgrass, further
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ANDREW D. IRVING AND MARK D. BERTNESS
Ecology, Vol. 90, No. 11
Does peat facilitate forb success?
Removing cordgrass shoots showed that the peat base
still had a substantial positive effect on forbs. Similar
responses occurred between sites, so data were combined
for final analysis. Survival of S. linearis seedlings was
greatest where shoots remained intact (;110%, more S.
linearis emerged after the experiment was established),
yet survival where shoots were removed was still
reasonable at ;62%, and certainly distinct from nearby
interbed regions where no forbs were found (Fig. 4a;
ANOVA on final day across sites, F2,27 ¼ 27.55, P ,
0.0001; SNK tests, shoots and peat . peat only .
interbed). Removing cordgrass shoots did not influence
adult S. linearis, with survival in the presence and
absence of shoots sampled at ;52–66% across sites (Fig.
4b; ANOVA on final day, F2,27 ¼ 27.61, P , 0.0001;
SNK tests, shoots and peat ¼ peat only . interbed).
FIG. 3. Effects of cordgrass shoot density and height
manipulations on S. linearis (a) seedling biomass, (b) adult
biomass, and (c) number of seeds produced. Data shown are
mean þ SE.
reducing biomass by 72% when cordgrass was short
(Fig. 3a; ANOVA density 3 height interaction, F1,16 ¼
4.98, P ¼ 0.0403; SNK tests, dense and tall ¼ dense and
short . sparse and tall . sparse and short).
FIG. 4. Effects of cordgrass shoot removal on the mean
(6SE) survival of S. linearis (a) seedlings, and (b) adults.
Similar trends were observed between sites so data were pooled.
Day 0 corresponds to the beginning of the experiment (early
May for seedlings and late June for adults). Note that survival
may exceed 100% as more S. linearis emerged after the
experiment was established.
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TABLE 2. A summary of the experimental effects of cordgrass shoot removal on S. linearis
seedling biomass, adult biomass, and number of seeds produced.
Response variable
Shoots and peat
Peat only
Seedling biomass (g dry mass)
Adult biomass (g dry mass)
Number of seeds per plant
0.180 6 0.014
4.519 6 0.366
465.90 6 56.52
0.071 6 0.011
1.526 6 0.294
163.44 6 42.86
Note: Values shown are means 6 SE.
At both sites, removing cordgrass shoots reduced per
capita S. linearis seedling biomass by ;60%, adult
biomass by 66%, and seed production by 65% (Table 2;
ANOVA, F1,18 ¼ 38.44, P , 0.0001 for seedling biomass;
F1,18 ¼ 40.60, P , 0.0001 for adult biomass; and F1,18 ¼
18.18, P ¼ 0.0005 for seed production).
Water flow and cobble stability measurements
For the test of cordgrass density and height, water
flow increased behind sparse cordgrass (25–32% greater
dissolution of plaster; ANOVA, density effect, F1,16 ¼
50.92, P , 0.0001), but was unaffected by cordgrass
height (ANOVA, height effect, F1,16 ¼ 3.74, P ¼ 0.0709).
Cobble movement was negligible in this experiment
(0.08–0.36 cm of movement), and did not statistically
differ among treatments (the greatest likelihood of
statistical significance was for density; ANOVA, F1,16
¼ 3.18, P ¼ 0.0933). However, both water flow and
cobble movement ranked as greater behind short
cordgrass (see Appendix C), and may therefore still
explain the observed effect of height on S. linearis
seedlings (Figs. 2a and 3a).
For tests of peat contribution, water flow was greatest
in interbed habitats (57–65% dissolution of plaster), less
behind peat (53%), and even less behind cordgrass
shoots (47–49%; ANOVA, F2,15 ¼ 23.76, P , 0.0001 at
Providence Point; F2,15 ¼ 112.48, P , 0.0001 at
Haffenreffer; SNK tests, shoots and peat , peat only
, interbed at both sites). Cobble movement was
negligible whether cordgrass shoots were removed or
not (0.3–1.6 cm of movement) but increased to 6.2–11.8
cm in interbed habitats (ANOVA, F2,12 ¼ 10.58, P ¼
0.0022 at Providence Point; F2,12 ¼ 4.72, P ¼ 0.0308 at
Haffenreffer; SNK tests, shoots and peat ¼ peat only ,
interbed at both sites).
DISCUSSION
Facilitation as a process affecting the distribution and
abundance of plants and animals was considered a
century ago (Clements 1916), but has only recently
received attention from researchers. Consequently, there
are many questions about facilitation and its importance
relative to the better studied processes of competition
and predation. Among these, understanding how traits
of a foundation species modify its positive effects on
associated species is key, since the very occurrence of
facilitation may depend on specific traits (Bruno and
Kennedy 2000). Using cobble beach cordgrass beds, a
habitat known to facilitate both terrestrial plant and
marine invertebrate communities (Bruno 2000, Altieri et
al. 2007), we have shown that the population-level traits
of cordgrass shoot density and height modify its
facilitative properties.
Foundation species such as trees, grasses, seagrasses,
and kelps often form extensive habitats but vary
substantially at smaller (patch) scales in traits such as
density and height. On cobble beaches, forb abundance
correlated positively with cordgrass shoot density and
height (Fig. 1a, b), and experimental manipulation of
these two traits demonstrated consistently strong effects
of shoot density on forb survival, biomass, and seed
production. Effects of shoot height were comparatively
minor, suggesting that cordgrass shoot density plays a
greater facilitative role than shoot height over the life
cycle of forbs.
In other habitats, population density is an important
structural feature that can affect the abundance of
associated species. For example, the density of fish can
be positively related to the density of plants within
subtidal forests of macroalgae (e.g., kelps; Anderson
1994, Levin and Hay 1996). In seagrass beds, fish and
shrimp density can increase with plant density (Fonseca
et al. 1996), possibly because greater densities of
seagrass shoots offer greater protection from predators
(Orth et al. 1984). Density is even important for
maintaining species richness and abundance of softsediment infauna within habitats created by tubebuilding polychaetes (Woodin 1978). Collectively, these
results suggest that density may be a key and general
population-level trait that can modify facilitation by
many foundation species.
There may also be some generalities in the mechanism(s) by which density modifies facilitation. In this
study, water flow and cobble movement were least
behind dense cordgrass, agreeing with previous studies
(Gleason et al. 1979, Leonard and Luther 1995), and
suggesting that cordgrass density modifies facilitation of
forbs through the primary mechanism identified by
Bruno (2000; i.e., reduced flow and stabilized cobbles).
Reduced flow at increased densities occurs among other
aquatic foundation species, such as kelp forests (Eckman et al. 1989) and seagrass beds (Eckman 1987), and
can affect the type and abundances of species facilitated
(Eckman 1987, Grizzle et al. 1996) as well as the
physiology and recruitment of the facilitator (Dennison
and Barnes 1988, Eckman et al. 1989). Analogous
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Ecology, Vol. 90, No. 11
PLATE 1. Photograph showing the spatial arrangement of a typical cobble beach plant community. Cordgrass shoots (Spartina
alterniflora) can be seen on the right (seaward), with a dense population of facilitated forbs growing to the left of the cordgrass. The
photograph was taken late in the growing season (3 August 2006) at Providence Point on Prudence Island, Rhode Island. A color
version is available in Appendix A. Photo credit: A. D. Irving.
examples can be found for wind in terrestrial forests
(Jones et al. 1994). As noted above, greater plant
densities can also inhibit predator/herbivore foraging
and thereby provide a refuge from consumption for prey
(Crowder and Cooper 1982, Orth et al. 1984), though
such effects appear irrelevant for cordgrass–forb facilitation because herbivory appears negligible in this
system (Bruno 2000, Kennedy and Bruno 2000). The
consequences to facilitation of other factors commonly
affected by density (e.g., temperature, light intensity,
desiccation stress; Bertness et al. 1999) are largely
unknown.
In addition to the influence of cordgrass shoots, we
found that the peat base makes a substantial contribution to forb facilitation across the growing season.
Removing shoots to leave only peat did not reduce forb
seedling survivorship to zero as is characteristic of
nearby interbed habitats, but instead maintained the
strength of facilitation at ;40–50% of treatments where
shoots remained intact (Fig. 4). Bruno and Kennedy
(2000) previously suggested that peat and shoots act
synergistically to reduce physical disturbance and
enhance facilitation of forbs. While our experiment
was not designed to detect this synergy, as such an
experiment would require orthogonal combinations of
the presence and absence of cordgrass shoots and peat,
our results nevertheless show that the peat itself plays a
role in the cordgrass–forb facilitation. Since cordgrass
beds are primarily peat when forbs emerge (March–
April), peat may be particularly important for facilitating forb establishment before cordgrass shoots can grow
and further ameliorate stress. Indeed, sampling of forb
seedling emergence revealed that substantial cordgrass
shoot biomass is not a prerequisite (see Appendix D).
For any foundation species, numerous traits are likely
to influence facilitation. As such, it may be possible to
predict the strength of facilitation in a hierarchical
fashion whereby successive trait thresholds are reached.
Using the current example, a cordgrass bed at least 25 m
long appears to be a primary trait threshold for forb
facilitation since the area behind smaller beds generally
remains unoccupied because small beds do not sufficiently ameliorate environmental stress (Bruno and
Kennedy 2000, Bruno 2002). Within these larger beds,
if cordgrass shoots are dense (;530 shoots per m2) then
forb facilitation is strengthened. However, if cordgrass is
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sparse (;250 shoots/m2), forb facilitation may be
enhanced behind tall cordgrass (;75–90 cm), but not
behind short cordgrass (;30–40 cm; Figs. 2 and 3).
With more research, other traits such as bed orientation,
width, and peat height could also be included. We expect
that similar predictive hierarchies exist for other systems
structured by foundation species.
Foundation species vary in their expression of traits,
ensuring that the amount of habitat/resources provided
and the degree of environmental modification varies
substantially over multiple scales of space and time. In
short, not all foundation species, or even patches of a
single foundation species, are created equal. This
understanding can help us predict where and when
facilitation may be strong or weak, but is also important
for developing conservation strategies. It has been
argued that protecting foundation species as habitat is
a better strategy for maximizing preservation of
biodiversity than individually targeting the inhabiting
species, but merely protecting a foundation species is not
adequate if threshold levels of particular traits must be
met (Bruno and Bertness 2001). For example, efforts to
restore salt marsh using short-form cordgrass failed to
attract the conservation target species, endangered
Light-footed Clapper Rails, because they prefer tallform cordgrass (Malakoff 1998). Clearly, understanding
the role of traits for facilitation can increase the
likelihood of success for important but expensive and
time-consuming conservation efforts.
Facilitation through habitat provision and environmental modification is a fundamental process affecting
the distribution, abundance, and diversity of life, yet
there is still much to learn because ecologists have only
recently become interested in positive species interactions (Bruno and Bertness 2001, Grutter and Irving
2007). For a comparatively well-understood interaction
(cordgrass–forb facilitation), we have shown how
variation in two common population-level traits of
foundation species can substantially modify its capacity
to facilitate. Such information not only builds upon our
theoretical understanding of facilitation as an ecological
process, but also highlights that the strength or even
occurrence of facilitation cannot be assumed just
because a foundation species is present. Further work
will likely identify cross-system consistencies that lend
themselves to the development of general ecological
theories that explain spatial and temporal variation in
facilitation, and the resulting effects on population
dynamics and community structure.
ACKNOWLEDGMENTS
The field assistance of K. Bromberg, T. Elsdon, W. Goldenheim, C. Holdredge, F. Jackson, P. Rix, B. Russell, and N.
Sala is greatly appreciated. We thank the Narragansett Bay
National Estuarine Research Reserve and Brown University’s
Haffenreffer Reserve for access to study sites and for their
continued support of ecological research. Sage advice from J.
Bruno helped shape the research, while D. Balata, K.
Bromberg, T. Elsdon, and two anonymous reviewers provided
constructive comments that improved the manuscript. This
3049
research was supported by Rhode Island Sea Grant and the
National Science Foundation.
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APPENDIX A
A color version of Plate 1, showing a typical cobble beach plant community (Ecological Archives E090-218-A1).
APPENDIX B
Bonferroni-Holm adjustments (Ecological Archives E090-218-A2).
APPENDIX C
Effects of cordgrass shoot density and height on water flow and cobble movement (Ecological Archives E090-218-A3).
APPENDIX D
Patterns in the emergence of cordgrass and forbs on cobble beaches (Ecological Archives E090-218-A4).