Download Habitat destruction and metacommunity size in pen

Journal of Animal Ecology 2008, 77, 1175–1182
doi: 10.1111/j.1365-2656.2008.01444.x
Habitat destruction and metacommunity size in pen shell
communities
Blackwell Publishing Ltd
Pablo Munguia*,‡ and Thomas E. Miller†
Department of Biological Science, Florida State University, Tallahassee, FL 32306–1100, USA
Summary
1. In spatially structured communities, habitat destruction can have two effects: first, a main effect
that occurs because of the loss of habitat area within a larger region, and a secondary effect due to
changes in the spatial arrangement of local communities. Changes to the spatial arrangement can,
in turn, affect the migration and extinction rates within local communities.
2. Our study involved the experimental destruction of entire local communities within larger
regions in natural marine microcosms. Large and small arrays of dead pen shells were created in a
shallow bay in north Florida, and the colonization by both encrusting and motile species on this
empty substrate were followed through time. After most species had become established, half of the
large arrays were perturbed to create small arrays by removal of half the shells, simulating habitat
destruction.
3. After 48 days of further community development, comparisons of the large arrays, reduced
arrays and original small arrays suggested that the mechanisms by which habitat destruction affects
diversity could depend upon the size of the region affected and the natural history of the species
being studied.
4. Habitat destruction reduced the diversity of motile species to a level lower than that found in the
undisturbed small arrays, suggesting that the species that assembled in the original large metacommunities negatively influenced the species that occurred ultimately in the converted small arrays.
5. With sessile species, habitat destruction created richness levels that were intermediate to those of
small and large arrays. The initial predestruction richness appears to have had a positive effect;
because sessile species cannot disperse as adults, they may not respond to significant shifts in
metacommunity size later in succession. Initial metacommunity size may be important for allowing
individuals to select appropriate habitats before they settle.
Key-words: abundance and distribution patterns, disturbance, diversity, fragmentation, marine
habitats, rare species
Journal of Animal Ecology (2007) doi: 10.1111/j.1365-2656.2007.0@@@@.x
Introduction
Habitat destruction is the primary explanation for the rapid
loss of biodiversity in many habitats over the last century –
for example, coral reefs have declined by an estimated 27%
because of pollution and human exploitation, and more than
78 million acres of tropical forest are estimated to be lost each
year to deforestation (Stone 1995; Gardner et al. 2003), with
accompanying losses to biodiversity (e.g. Roberts et al. 2002).
Despite these widespread effects, we still do not know the
mechanisms by which habitat destruction affects diversity
*Correspondence author. E-mail: [email protected]
†Present address: UMDI-Sisal, Fac. Ciencias, UNAM, Sisal-Hunucma,
Yucatan, Mexico, 97355.
‡Marine Science Institute, The University of Texas at Austin, 750
Channel View Drive, Port Aransas, TX, 78373, USA.
(Debinski & Holt 2000; Gonzalez 2005). It may act directly by
reducing available area: the positive relationship between
habitat area and the number of species in a habitat is well
known (MacArthur & Wilson 1967; Brown & Lomolino
1998). However, destruction may also have significant
secondary effects by changing the spatial structure of populations and communities (Tilman et al. 1994; Gonzalez et al.
1998; Gonzalez 2005).
Disturbance can occur at different spatial and temporal
scales, with consequences for the resulting community
patterns (e.g. Miller 1982). A common ecological scenario is
the effect of localized disturbances creating small patches of
destruction within a larger matrix of an established community (e.g. by Connell 1978; Paine & Levin 1981). When
disturbance occurs on a greater scale (i.e. larger or more
frequent disturbances), it can result in a large community
being broken down into smaller units (fragments; Collinge
© 2008 The Authors. Journal compilation © 2008 British Ecological Society
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P. Munguia & T. E. Miller
2000; Gonzalez 2000; Fahrig 2003). If the habitat is already
spatially structured (or has been fragmented), such that
established smaller ‘local’ communities occur as patches, then
large-scale destruction can eliminate entire local communities,
affecting both the density and distance among local patches
(Gonzalez 2005). Habitat destruction thus has two effects;
first, a main effect that occurs because of the loss of area in a
habitat, and a secondary effect due to the change in the spatial
arrangement of communities. Changes to the spatial arrangement can, in turn, affect the migration rates among fragments
and the extinction rates within individual fragments. This
secondary effect will be most important in systems where
migration strongly affects diversity (Callum 1997). In communities undergoing habitat fragmentation, the movement of
individuals from one patch to another has been considered an
important mechanism controlling populations and diversity
(Debinski & Holt 2000).
Metapopulation theory has been used to explain how
sources and sinks allow species persistence in habitat
fragments (e.g. Gonzalez et al. 1998; Mouquet & Loreau
2003). Similarly, habitat destruction involves the removal of a
local community (or fragment, if the community is already
fragmented) from the environment and may be particularly
important when local communities are linked to one another
through migration (i.e. form a metacommunity; Leibold &
Miller 2004). One of the proposed outcomes of such habitat
destruction is an extinction debt (Tilman et al. 1994), which
suggests that asynchronous population dynamics in sources
and sinks will cause a reduction in diversity some time after
habitat destruction takes place. Other outcomes could
include the modification of the abiotic habitat or the loss of
habitat heterogeneity, both of which could have potentially
negative effects on diversity.
We can understand the effects of habitat destruction on
diversity by considering how local diversity changes with
succession, habitat area and fragmentation (Mouquet et al.
2003). New habitats are expected to gain species through time
up to some asymptote, with larger metacommunities (i.e.
those with more local communities) supporting more species
than smaller ones, either because of the species–area relationship
(Connor & McCoy 1979) or because there are more habitats
that offer refugia and heterogeneity to a larger suite of species
(Leibold et al. 2004; Mouquet et al. 2006). The reduction in
the number of local habitats through habitat destruction
might therefore have one of three effects on diversity. First,
the null expectation is that diversity might simply decrease to
a level appropriate to the new metacommunity size. Secondly,
the effects of a small metacommunity and some effect of the
destruction itself on the spatial or landscape pattern (e.g.
extinction debt) might combine to produce a diversity lower
than that expected from the new metacommunity size (we call
this a negative residual effect). Thirdly, species from the
original larger metacommunity might persist, resulting in a
new diversity level somewhat higher than that expected from
the new metacommunity size (a positive residual effect). This
last response can occur due to historical processes during
community formation; positive species interactions at the
local scale may allow species persistence after destruction.
Alternatively, high rates of dispersal may counter local
extinctions and allow species persistence even after habitat
destruction has taken place (e.g. rescue or mass effects,
Leibold et al. 2004).
Destruction of local communities can also affect the
patterns of species’ relative abundance. Studies have demonstrated a positive relationship between local abundance and
regional distribution (Brown 1984; Gaston, Blackburn &
Lawton 1997), so most species are believed to be on a continuum between locally rare and having narrow distributions
to locally abundant and having broad distributions. This
abundance–distribution relationship may change, however,
with successional patterns (Mouquet et al. 2003), as well as
with mechanisms such as habitat destruction that affect
whole communities. Following habitat destruction, some
species may increase their distribution or local abundance,
while others will decline, depending on species-specific responses
to disturbance (Mouquet & Loreau 2003; Shurin et al. 2004).
We used the natural communities of small marine
invertebrates found living in empty pen shells as experimental
microcosms (see, e.g. Srivastava et al. 2004) to test the effects
of metacommunity size and habitat destruction on local
diversity and species commonness and rarity. Pen shell
communities are a useful system for testing scaling issues in
diversity (Munguia 2004), because each shell can be considered
as a discrete habitat among a seagrass matrix where many
species experience these habitats as metapopulations
(Munguia, Mackie & Levitan 2007). In particular, we test
whether small metacommunities have similar diversity levels
as large metacommunities, and test if a shift in community
density (number of habitats per unit area) through destruction
will change diversity in different types of pen shell species.
Then, we test whether the effect of habitat destruction is
simply a reduction of habitat area or if it is a reduction of the
species pool in that particular region. We also compare
changes in species’ habitat occupancy and local abundance
through successional time to determine whether species
responded similarly to habitat destruction.
Methods
Our study was carried out in the summer of 2003 in St Joe Bay,
Florida, a shallow, well-protected bay on the northern Gulf of
Mexico. The substrate is composed of patches of sea-grass beds
intermixed with sandy areas; very few natural hard surfaces are
available other than the empty shells of dead pen shells Atrina rigida
(Lightfoot). Pen shells are relatively large bivalves (~19 cm length)
that live embedded in the sand within sea-grass beds. The shells
remain in the sand once the mollusc dies, providing habitat for a
large number of invertebrates and fish that are generally not found
in the areas surrounding pen shells (Munguia 2004, 2007). The
approximately 70 species occurring on dead pen shells experience
processes at three discrete spatial scales: within an individual shell,
where species interactions such as competition and predation
generally occur, among neighbouring shells where individuals may
move during their lifetimes (which we will define operationally as
within the pen-shell metacommunity) and a much larger spatial scale
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Animal Ecology, 77, 1175–1182
Habitat destruction in metacommunities
Fig. 1. Experimental design of the habitat destruction study. Top:
three treatments of different densities were used: a large array (L)
consisting of 16 shells, a small array (S) of four shells and a habitat
destruction array (D) comprised of 16 shells, of which 12 shells were
removed during community formation (dark circles). Bottom: during
each sampling period, shells had to be sampled destructively;
therefore there were replicates for each sampling date. At the 21-day
collection time the destruction treatment was still equal to the large
treatment, so we used the shells that were ‘destroyed’ as samples to
estimate diversity in the destruction arrays (hence the ‘large’ box
surrounding the D). Four blocks contained one array for each
collection time, and four blocks contained one array that was
collected at the last sampling time. The design had more power at the
last sampling date (eight blocks) than when we first sampled (four
blocks).
1177
evenly spaced shells and one small square array consisting of four
shells, keeping the distance between shells constant (40 cm) within
each array (Fig. 1, top). All the shells that were anchored were empty
and fouling-free and of relatively the same size (average of 20 cm in
length), allowing us to follow natural succession patterns (see
Munguia 2004). In order to quantify all the species occurring on pen
shells on any given sample date, shells had to be sampled destructively.
Sampled shells were brought to the surface using sealed bags
preventing the loss of organisms, and then taken to the laboratory
for identification and quantification of inhabitants larger than
1 mm2 in size. This procedure does not affect neighbouring shells, as
disturbance to the surrounding habitat is minimal, and species tend
to remain within the refuge of the pen shell. After 21 days, 12 shells
were removed from one of the two large arrays on each plot, leaving
an array of four neighbouring shells: two shells that were on the
outside of the original array and two on the inside, in order to
account for potential edge effects. Within each plot, the large array
represented the ‘large metacommunity’ treatment, the small array
the ‘small metacommunity’ treatment and the reduced array the
‘habitat destruction’ treatment (Fig. 1, bottom). We defined the
species pool as the species that were found at the scale of the entire
array of four or 16 shells (an array therefore becomes a metacommunity),
and local diversity was defined at the scale of a single shell within an
array. Habitat destruction occurred at mid-succession, when all
species in the species pool were present on at least some shells in the
array (Munguia 2006). This timing allowed the effects of both habitat
destruction and community age (Mouquet et al. 2003) to occur in
our experiment.
We established these arrays in eight areas chosen randomly within
St Joe Bay. Four of these areas contained three arrays of each
treatment type, one for each collection time, and four of these areas
contained only one array of each type, which was collected at the last
sampling time (Fig. 1, bottom). At 21 and 63 days after deployment
of the arrays, one array of each treatment was collected for censusing
of species present (n = 4 for 21 days, n = 8 for 63 days). Previous
experiments on succession in pen shell communities (Munguia 2004,
2006) have demonstrated that this time-period (63 days) was sufficient
for empty shells to be colonized and approach some relatively stable
near-equilibrium state.
CHANGES IN LOCAL SPECIES RICHNESS
at which reproductive propagules may disperse (including the entire
bay and possibly parts of the Gulf of Mexico). For analyses, we
divided species found on pen shells into two groups based on their
ability to move among shells within a metacommunity. Motile
species, such as crustaceans and fishes, can move among communities
as juveniles and adults, whereas sessile species, such as barnacles and
bryozoans, have limited motility and generally move among communities only as propagules (Munguia 2004, 2007). The majority of
motile species are found only on pen shells, but show random distribution
patterns. However, there are few motile species that aggregate within
shells (i.e. very abundant when present), such as the shrimp Palaemon
floridianus (Chace) and the amphipod Dulichiella appendiculata
(Say); in contrast, most sessile species show clumped distributions
(Munguia 2007). Therefore, the fate of the habitat has the potential
to cause different responses by species with these distribution patterns,
particularly when species can have different stage-dependent
dispersal strategies (Munguia et al. 2007).
Replicate plots of three arrays of anchored pen shells were established
within eight 2·25 m2 areas: two large square arrays consisting of 16
To address the primary question of the effects of destruction on
species richness, we compared local diversity among all three
treatments. Four shells from each of the large arrays that had the
same position within their array as the habitat destruction treatment
were used for statistical comparisons with the other two treatments,
so that sample sizes and positions would be as similar as possible.
Species richness of the three treatments was compared at each collection
time by analysis of variance, treating plots as a blocking effect to
account for variance due to spatial location.
REDUCTION IN HABITAT AREA EFFECTS
After quantifying the effects of destruction, we then tested two
potential sources through which habitat destruction might affect
species richness: the reduction of habitat area and the reduction of
the species pool in that particular region. If destruction is simply a
change in habitat area through decreasing the number of local
communities (i.e. pen shells), then the size of the available pool of
species should also decrease. We compared the regional richness
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Animal Ecology, 77, 1175–1182
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P. Munguia & T. E. Miller
from the large array treatment (all 16 shells within an array for all
eight sites), a simulated small array treatment (using data drawn
from four subsampled shells from the 16-shell array) and the
destruction treatment (four shells). Because of differences in sample
size, and because the values in the subsample were part of the large
array treatment, we tested these differences by bootstrapping
regional richness of the large arrays (2000 iterations of 16 shells per
site per treatment); the regional diversity of the small arrays were
also bootstrapped for reference. Using the 95% confidence intervals
across sites, we tested for the significance of the difference between
two treatments with Tukey’s procedure (Zar 1999). If the confidence
intervals crossed zero (i.e. difference between means is not different
from zero), then the two compared treatments were not different
from one another.
Our a priori hypothesis was that regional diversities would vary in
the following fashion: first, if regional diversity in the large array
differed from the simulated small array, and this one in turn was
similar to the diversity found in the habitat destruction treatment,
then we would assume that the effect of habitat destruction is due
simply to the reduction in area associated with the removal of pen
shells. Alternatively, if regional diversity in the large array was
similar to the diversity in the simulated small arrays, and the diversity
in the simulated small arrays differed from the diversity in the habitat
destruction treatment, then we would assume that habitat destruction
has an additional effect on the species pool over and above that due
to the loss of area associated with the removal of pen shells.
CHANGES IN COMMONNESS AND RARITY
For each colonizing species, the mean number of shells (habitats)
occupied in each plot for each treatment was compared with the
maximum local abundance in a plot for that species. Similar comparisons
have been conducted previously in other systems at a single sampling
time (Brown 1984; Gaston et al. 1997). In our analysis, we plotted
the abundance against the distribution for each species for the first
and last sampling dates, creating a vector between the two dates. We
then standardized all the species vectors by setting the first collection
point to zero; the vectors therefore reflected the direction and
magnitude of change in local abundance and the number of shells
occupied. In order to avoid pseudoreplication, we averaged all the
vectors for each species within a treatment across the replicates, and
then averaged across species to make comparisons among treatments.
Changes in both abundance and proportion of shells occupied were
subjected to angular transformation, and we compared all possible
pairs of the average vectors for the three treatments using a
non-parametric two-sample second-order analysis of angles (Zar
1999).
Fig. 2. Species richness pre- and post-habitat destruction was
implemented for motile (a) and sessile (b) species. Open bars
represent small arrays of local communities (four communities), grey
bars represent large arrays (16 communities) and black bars represent
arrays that underwent habitat destruction (a shift from 16 to four
communities). Bars are treatment means with one standard error;
different letters represent statistically different levels of species
richness (P < 0·05; Tukey’s honestly significant difference test); there
were no predestruction treatment differences.
Similarly, sessile species had similar local richnesses at
21 days (F = 1·07, P > 0·31). Species diversity in all three
treatments continued to increase from day 21 to day 63 after
the implementation of habitat destruction (Fig. 2b), but they
differed significantly in species richness at 63 days (F = 5·37,
P = 0·008). At the end of the experiment, richness in the
undisturbed large array treatment was greater than in the
small arrays, with the habitat destruction treatment having an
intermediate level between the two.
Results
REDUCTION IN HABITAT AREA EFFECTS
CHANGES IN LOCAL SPECIES RICHNESS
Motile species richness in local communities increased with
time in both large and small metacommunities: at 21 days,
richnesses were not significantly different among the large
and small arrays and the habitat destruction treatments prior
to destruction (F = 1·49, P > 0·23; Fig. 2a). By the final
sample (day 63), the treatments diverged in species richness
(F = 7·09, P < 0·0001), both the large and small arrays had
similar levels of diversity, while the habitat destruction
treatment had lower diversity.
Changes in regional species richness are due to more than
simply changes in the number of local communities, based
upon an inspection of the 95% confidence intervals from the
bootstrapped values across the large array (L; considering a
16-shell sample), simulated small array (Ls; four-shell sample
of the 16 shells) and destruction (D; four-shell sample)
treatments (Fig. 3). Regional diversity of pen shells in the
habitat destruction treatment appears to drop a couple of
species due to changes in species pool size and in the number
of habitats. Further, the destruction treatment presents less
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Animal Ecology, 77, 1175–1182
Habitat destruction in metacommunities 1179
Fig. 3. Bootstrapped species richness values for both motile and
sessile species for the last sampling date (63 days). Open circles
represent large arrays, shaded triangles simulated arrays and closed
circles arrays subjected to ‘habitat destruction’; open triangles
represent small arrays and are shifted to the right for clarity. Error
bars are 95% confidence intervals; lack of overlap in error bars
suggests differences between groups.
variation in the number of species than the simulated small
array and the actual small array.
CHANGES IN SPECIES COMMONNESS AND RARITY
In large metacommunities over time, motile species tended to
increase in proportion of habitats occupied as well as in local
abundance (Fig. 4a). In small metacommunities, the proportion
of habitats occupied by each motile species decreased over
time, but local population abundances actually increased.
Local diversity in small arrays can therefore reach levels
expected for larger arrays. Habitat destruction generally
caused populations to experience lower population growth
than did those in the large and small metacommunities and
therefore little change in the relationship between abundance
and habitat occupancy (Fig. 4a). Each of the treatment
vectors was significantly different from the others [two-sample
analysis of vectors: large and small arrays, degrees of freedom
(d.f.) = 43,46, U2 = 0·46, P < 0·01; large and habitat-destruction
arrays, d.f. = 43,50, U2 = 0·75, P < 0·01; small and habitatdestruction arrays, d.f. = 46, 50, U2 = 0·60, P < 0·01].
Sessile species increased in both local abundance and
number of habitats occupied over time in all three treatments
(Fig. 4b), but the magnitudes of increase differed; increases
were greatest in large arrays and smallest in small arrays
(two-sample analysis of vectors: large and small arrays,
d.f. = 19,20, U2 = 0·44, P < 0·01; large and habitat-destruction
arrays, d.f. = 19,21, U2 = 0·78, P < 0·01; small and habitatdestruction arrays, d.f. = 20,21, U2 = 0·45, P < 0·01). As with
motile species, the habitat destruction correlated with lower
rates of growth and habitat spread (Fig. 4b).
Fig. 4. Species abundance–distribution trajectories under succession
from the field experiment for (a) motile and (b) sessile species. Open
circles represent large arrays, triangles small arrays and closed circles
arrays subjected to ‘habitat destruction’.
Discussion
Results from our study suggest that habitat destruction can
have complex effects on local community structure. For some
types of species, destruction reduces available area, leading to
a decrease in richness as described by species–area relationships.
However, there are also secondary effects of successional history
or the deleterious effects of destruction that affect the response
of a community to habitat destruction. The regional species pool
for both motile and sessile species was reduced under habitat
destruction by only a couple of species. This small reduction in
species pool suggests that habitat destruction is affecting local
diversity much more strongly than regional diversity in pen
shell communities. Furthermore, the effects of area alone and
the effects of secondary mechanisms on diversity will vary
depending upon whether species involved are motile or
sessile.
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Animal Ecology, 77, 1175–1182
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P. Munguia & T. E. Miller
Local richness of motile species in large arrays increased as
the community underwent succession (Fig. 2a). Contrary to
our expectations, small arrays reached the same level of
richness, suggesting that there was no significant increase in
richness with metacommunity area for these species. In large
arrays subjected to habitat destruction during succession,
however, richness was lower than in either the unmanipulated
large or small arrays. However, the species pool was not
affected severely by the destruction treatment; rather, the
distribution of individual motile species and local diversity
was mainly affected. Therefore, habitat destruction had a
secondary, negative, effect on the number of motile species,
suggesting that the species that assemble in large arrays
dominate or otherwise affect negatively the communities that
occur in the small arrays created through habitat destruction.
The number of sessile species in both small and large arrays
also increased through the last sampling date, with a lower
local richness in small arrays (Fig. 2b). This result is consistent
with our expectation that the initial metacommunity size
should influence species richness. Arrays subjected to habitat
destruction achieved richness levels that were intermediate
between those of the original small and large arrays. The
initial predestruction richness appears to have had a positive
secondary effect on the sessile species richness after destruction.
Because sessile species cannot disperse as adults, they may not
respond to significant shifts in metacommunity size, such as
occur with destruction – and this is reflected in the weak
ecological effects observed. Alternatively, sessile species may
be subject to a mechanism similar to the extinction debt
(Tilman et al. 1994) due to a slower response by sessile species’
populations. Initial metacommunity size may be important
for allowing individuals to select appropriate habitats before
they settle (Mouquet & Loreau 2003). However, once these
individuals are established, their presence may suppress
incoming recruits, suggesting that priority effects could be
important for this species group (see, e.g. Tilman, Lehman &
Yin 1997; Almany 2003; Fukami 2004; Munguia 2004).
H A B I T A T D E S T R UCT ION AND REGIONAL SPECIES P OOLS
Habitat destruction also affected the regional species pool of
potential colonizers. Both motile and sessile species pools
were significantly different between the destruction treatment
and the simulated small array. The reduction of number of
habitats available had direct effects on the number of potential
colonizers, independent of the size of the metacommunity
array. Motile species diversity was not affected by array size,
but rather by the direct effect of destruction that, in turn,
reduced the species pool. Motile species, such as the amphipods
D. appendiculata and Bemlos unicornis (Bynum and Fox), may
have tracked available habitats (Munguia 2007; Munguia
et al. 2007); therefore, a reduction in habitats had the potential
to affect source populations. However, not all species responded
the same way to habitat destruction; for example, the hermit
crab Pagurus sp. was affected mainly by the original array size,
having larger populations in the destruction and large arrays
than in the small arrays; while the isopod Paracerceis sp.
maintained higher populations in the destruction and small
arrays than in the large arrays. Finally, the amphipod Melita
nitida S. I. Smith showed a much higher abundance in the
destruction treatment than in the large and small arrays,
which could be due to the nomadic nature of this species
(Munguia et al. 2007). Sessile species diversity was affected
by the initial array size; the reduction of the species pool is
linked probably to the number of habitats available. This
pattern could have occurred because species such as the
ascidian Didemnum sp. and the sponge Haliclona sp.
require hard substrate to settle and grow, and their distribution patterns are similar to the distribution of pen shells
(Munguia 2007).
ABUNDANCE–DISTRIBUTION RELATIONSHIP
In our experiment, habitat destruction is related to lower pen
shell occupancy, due perhaps to lower migration of motile
species among shells relative to the undisturbed large and
small metacommunities. Destruction may have caused a
reduction of potential sources for motile species which may,
in turn, reduce the likelihood that a local population would
serve as a source and seed neighbouring localities. Changes in
species distribution among local habitat (shells) differed
among the three treatments (Fig. 4a). Smaller arrays had
lower local diversity, perhaps because of increased species
interactions or lower rates of migration from fewer sources.
Motile species may be sorting themselves out among habitats,
with lower richness on each local habitat (Sale 1977; Leibold &
Miller 2004), and a reduction of habitats increases the likelihood of a species from being excluded from the group of habitats.
Changes over time in sessile species distribution and
abundance suggest that short-distance dispersal is important
for some of these species (Olson 1985; Bingham & Young
1991) and that communities at high densities therefore
showed high species richness (Fig. 2b). Sessile species were
not affected by metacommunity size or habitat destruction
because the adults could not disperse: they had similar
population-growth patterns and distributions in all arrays
(Fig. 4b). Successional changes in sessile species were
independent of the size of the metacommunity once the initial
colonization pattern had occurred. What is interesting to note
is that the initial assembly or colonization pattern (Belyea &
Lancaster 1999) can affect local diversity but not the increase
in abundance or distribution of individual species.
The metacommunity concept seems especially appropriate
for the communities associated with pen shells, as the shells
define discrete spatial scales at which different processes may
occur (Munguia 2007). However, as with other studies that
attempt to relate local processes to regional mechanisms in
natural systems, delimiting relevant spatial scales is problematic
(Srivastava 1999; Munguia 2004). The possibility of very high
long-distance dispersal for some species found on pen shells
means that the community does not have a regionally closed
system, as is assumed in most metacommunity theory
(Leibold et al. 2004). It is likely that most natural metacommunities are not enclosed completely, at least at the scale that
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Animal Ecology, 77, 1175–1182
Habitat destruction in metacommunities
regional processes (such as dispersal and habitat heterogeneity)
are thought to operate. In pen shells, species respond to our
manipulations of metacommunity size, which suggests that
migration is important from neighbouring shells up to metres
away. However, there is probably a low propagule input from
larger scales, which could be crucial for establishing the first
colonizers in pen shell metacommunities. An important
question that would need to be addressed with natural
systems is how different spatial scales change the influences of
processes as communities undergo succession.
Our study supports recent theoretical studies showing that
the interaction between dispersal limitation, species interactions and habitat structure can affect diversity (Tilman
et al. 1997; Chesson 2000; Amarasekare et al. 2004). Clearly,
habitat destruction can have both main (through species–area
relationships) and secondary effects (positive or negative residual
effects) on community diversity. Species have different dispersal
rates, growth rates and competitive abilities, which contributed
to differences in abundance across treatments. In general, species
that are locally rare also occupy few habitats (Brown 1984;
Gaston et al. 1997) and may therefore also be more susceptible
to the effects of habitat destruction (Gonzalez et al. 1998).
The observed community patterns result from the different
responses of and interactions among component species.
The response of natural communities to habitat destruction
depends clearly upon the scales of the habitat, the destruction
and the species involved. Investigating patterns of species’
commonness and rarity (Magurran & Henderson 2003)
provides insight into changes in species abundances, suggesting
in particular that they are (a) dispersal-limited, (b) resourcelimited or (c) limited by species interactions (e.g. competition
and predation). Habitat destruction can affect any of these
parameters, but their combined effects can be understood
only in the larger, metacommunity context. Manipulating
whole communities has allowed us to study the interaction
between regional size, habitat destruction and their combined
effects on diversity.
Acknowledgements
We would like to thank Don R. Levitan, Andy Gonzalez, Brian D. Inouye,
Casey Terhorst and Dave Ferrell for comments to the manuscript, as well as
Kim Young for field assistance. K. Moriuchi assisted with the bootstrap
procedure. This research was funded by a COFRS grant from Florida State
University to T. E. Miller.
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Received 23 April 2008; accepted 22 May 2008
Handling Editor: Andy Gonzalez
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