Download Niche diversity in crustacean cryptic species

Oecologia (2007) 154:175–183
DOI 10.1007/s00442-007-0816-x
COMMUNITY ECOLOGY
Niche diversity in crustacean cryptic species: complementarity
in spatial distribution and predation risk
Gary A. Wellborn Æ Rickey D. Cothran
Received: 11 January 2007 / Accepted: 11 July 2007 / Published online: 8 August 2007
! Springer-Verlag 2007
Abstract Recent genetic studies indicate that species
with very close phenotypic similarity (‘‘cryptic species’’)
are a common feature of nature, and that such cryptic
species often coexist in communities. Because traditional
views of species coexistence demand that species differ in
phenotype to coexist stably, the existence of sympatric
cryptic species appears to challenge traditional perspectives of coexistence. We evaluated niche diversity in three
recently discovered species of Hyalella amphipods that
occur sympatrically in lakes and share close phenotypic
similarity. We found that, in some cases, these species
exhibited strong complementary spatial distributions within
the littoral zone of lakes, both across a distance-from-shore
gradient, and a vertical depth gradient. Additionally, we
compared fish stomach contents with habitat samples and
found that species differed in their vulnerability to predation from sunfish (Lepomis spp.). Complementarity among
species across axes of spatial distribution and predation
risk, two important niche components, suggests that species
with close phenotypic similarity may differ appreciably
along ecologically relevant axes. Our results, considered in
the light of previous studies, suggest a community structured by predator-mediated coexistence or sequential
dominance across environmental gradients in the littoral
zone.
Communicated by Carla Caceres.
G. A. Wellborn (&) ! R. D. Cothran
Department of Zoology and Biological Station,
University of Oklahoma, Norman, OK 73019, USA
e-mail: [email protected]
R. D. Cothran
e-mail: [email protected]
Keywords Hyalella ! Amphipoda ! Cryptic species !
Niche ! Coexistence
Introduction
Niche-based coexistence constitutes the conventional
foundation of community ecology, and the explanatory
power of the niche paradigm is well established (Tilman
1982; Chase and Leibold 2003). Nonetheless, a growing
number of recent genetic studies demonstrate that communities often harbor much hidden biological diversity in
the form of cryptic species (e.g., Gomez et al. 2002; Hebert
et al. 2004; Stuart et al. 2006; Witt et al. 2006). These
species may present a challenge to traditional views of
species coexistence (McPeek and Gomulkiewicz 2005;
Leibold and McPeek 2006) because it is not apparent that
these ‘‘cryptic species’’ (used here to refer to species with
very high phenotypic similarity) possess sufficient phenotypic and ecological disparity to foster coexistence through
niche differentiation. A variety of mechanisms have been
proposed to explain maintenance of diversity in communities of cryptic species. One potential mechanism is that
the species are functionally equivalent, or nearly so, but
can persist together through non-equilibrium dynamics
over long time scales (Hubbell and Foster 1986; McPeek
and Gomulkiewicz 2005). Alternatively, these species may
coexist through niche partitioning despite their high phenotypic similarity. Indeed, niche theory suggests that we
might often expect coexistence of species that are very
similar in traits that shape their responses to environmental
factors, provided appropriate kinds phenotypic tradeoffs
occur (Leibold 1998). Finally, when phenotypically similar
species interact in a metacommunity context, the distinction between niche and neutral mechanisms may be blurred
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176
because drift processes might shape species co-occurrence
at least as much as niche-based dynamics (McPeek and
Gomulkiewicz 2005; Leibold and McPeek 2006).
Currently, little is known about the mechanisms that
promote cryptic species diversity in communities (Molbo
et al. 2003; Zhang et al. 2004; Nicholls and Racey 2006).
Here, we report an initial study of ecological variation
among phenotypically similar amphipod species. Our goal
is to illuminate possible mechanisms that promote their
coexistence within the littoral zone of small North American lakes. We assess whether, and to what extent, species
differ in habitat use and predation risk, two niche axes that
commonly mediate competitive interactions in freshwater
communities (Werner and McPeek 1994; Skelly 1995;
Tessier and Leibold 1997). Although experimental studies
are ultimately required to determine causal processes promoting coexistence, our observational study suggests that
strong niche differentiation is possible among species with
very close phenotypic similarity.
Materials and methods
Study system
Amphipod crustaceans in the genus Hyalella are common
inhabitants of freshwater habitats throughout much of the
New World (Bousfield 1996). The North American radiation of Hyalella includes several geographically widespread species that exhibit much phenotypic similarity
(Wellborn et al. 2005), so much so that they had been long
considered a single widespread species called Hyalella
azteca. Recent genetic studies have revealed much hidden
biological diversity in the taxon (Witt and Hebert 2000;
Wellborn et al. 2005; Witt et al. 2006; Wellborn and
Broughton, in review). Current evidence suggests Hyalella
originated in South America, and invaded North America
roughly 8 million years ago, where they form a monophyletic clade with respect to South American representatives (Witt and Hebert 2000; Wellborn and Broughton, in
review). Except for some highly geographically restricted
endemic species, North American Hyalella have not been
formally described, and are known primarily through
genetic studies (Witt and Hebert 2000; Witt et al. 2006;
Wellborn and Broughton, in review).
Our study focuses on three undescribed species, referred
to here as species A, B, and C that co-occur in the littoral
vegetation of small lakes throughout the upper Midwest of
North America (Witt and Hebert 2000; Wellborn and
Cothran 2004). These species live on aquatic macrophytes
where they graze periphyton, and are all ‘‘small ecomorph’’
species (sensu Wellborn et al. 2005; Wellborn and
Broughton, in review). Total abundance of Hyalella in
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Oecologia (2007) 154:175–183
vegetated regions of these habitats is about 10,000 individuals m"2 (Wellborn 1994a). An earlier study (Wellborn
and Cothran 2004) demonstrated that these species are
reproductively isolated, and differ in mean values of some
traits, including body size, an ecologically important trait
in many freshwater species (Wellborn et al. 1996),
including Hyalella (Wellborn 1994a, 2002). Species B has
the largest mean adult body size, and is approximately,
13% larger in length than species A and 11% larger than
species C (Wellborn and Cothran 2004). Size distributions
of the full populations, including juveniles and adults,
overlap substantially (Wellborn and Cothran 2004).
Spatial distribution of species
We evaluated spatial distribution patterns of the three
species in two lakes during July 2002. Our approach was to
sample within major habitat types or regions within the
littoral zone of each lake. At Sullivan Lake, Michigan
(42"240 N, 84"030 W), we assessed the distribution of
Hyalella species along three transects oriented parallel to
the shore. One transect sampled the narrow edge habitat
within 0.5 m of the shore (depth < 0.1 m) where the substrate consisted of scattered Chara, detritus, and stems of
emergent sedges and other plants. Two deeper transects
sampled approximately 5 and 10 m from shore at depths of
approximately 0.4 and 1.0 m, respectively. The macrophyte community in the gradually sloping littoral zone was
composed of Chara mixed with Potamogeton and Myriophyllum in the 5 m transect, and Potamogeton and Myriophyllum in the 10 m transect. Along each transect we
collected 13–23 samples at 1- to 2-m intervals. In the two
deeper transects, we sampled haphazardly across depths
within vegetation. In the shallow edge habitat we collected
samples from small patches of Chara, on loose detritus,
and among stems of emergent plants. Sullivan Lake
samples contained 7.9 ± 1.10 (mean ± SE) individuals.
The littoral zone of Duck Lake, Michigan (42"290 N,
83"580 W) was dominated by Myriophyllum and Potamogeton that extended to the water surface, and we focused
primarily on species distribution within this habitat type.
We sampled along two transects parallel to shore, one
approximately 5 m from shore at a depth of about 0.5 m,
and the other 10 m from shore a depth of 1.0–1.5 m.
Additionally, within each of these transects, we collected
samples at two vertical depths: (1) in the upper few centimeters where the plant reached the water surface, and (2)
20–30 cm below the surface. Seven to twelve samples were
collected at each combination of distance from shore and
vertical depth. In addition to sampling the dominant habitat
type, we studied two kinds of habitats that were present,
but not common, in the littoral zone of Duck Lake. We
Oecologia (2007) 154:175–183
sampled the base of an emergent plant, arrow weed
(Sagittaria), that occurred along the transect 5 m from
shore (six samples). In the transect 10 m from shore, we
sampled the upper portion of Myriophyllum in areas where
the plant did not extend to the surface, terminating about
30 cm below the water surface (eight samples). Duck Lake
samples contained 6.7 ± 0.86 (mean ± SE) individuals.
To collect amphipod samples, we used small
(125 · 100 mm), fine-mesh dip nets to sweep through
approximately 10 cm of macrophytes, and emptied the
contents of each sample into white plastic trays, in which
all but the smallest juvenile amphipods were easily visible.
Amphipods were removed from trays using plastic pipettes,
and preserved in 95% ethanol. Because we are not aware of
any reliable morphological means of distinguishing species, all amphipods were identified to species using a
polymerase chain reaction (PCR)-based genetic analysis
that is described fully in Wellborn and Cothran (2004).
Briefly, a small amount of tissue (e.g., an appendage) was
removed from an individual for DNA extraction. PCR
reactions used primers designed to yield species-specific
products that identified species as length variants in gel
electrophoresis.
Analyses were conducted separately for the two lakes. In
Sullivan Lake, we first asked whether relative abundance of
Hyalella species differed across the three distance-fromshore transects. To evaluate this question we used multivariate ANOVA (MANOVA) with distance from shore as
the single factor. Dependent variables in the analysis were
angular-transformed proportions of species A and B in each
sample. The proportion of species C was not included
directly because proportions of all species within a sample
must sum to unity. Because the MANOVA revealed a significant overall effect, we used ANOVA to explore causes of
the effect in planned comparisons of the proportional abundance of each species across the three transects. For each
significant test, we then conducted pairwise tests for each
distance-from-shore combination, employing the Bonferroni
method to control type I error (Sokal and Rohlf 1995).
In Duck Lake, analysis focused on the dominant habitat
type, Potamogeton and Myriophylum that extended to the
water surface. We conducted a two-way ANOVA with distance from shore and vertical distribution (near surface and
20–30 cm below surface) as factors. Because species B was
almost entirely absent in the habitat samples, the dependent
variable in Duck Lake analyses was the angular-transformed
proportion of species A in a sample. Additionally, within
each transect we compared relative abundance patterns in the
dominant habitats (near surface and mid-depth in regions
where macrophytes extended to surface) with those of the
two less common habitats (base of arrow weed and habitats
where macrophytes did not extend to the surface). These
analyses used ANOVA to evaluate differences between the
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less common habitat and each of the dominant habitats at the
same distance from shore.
Predation risk
We evaluated risk of fish predation for the sympatric cryptic
species in both Duck Lake and South Lake (42"240 N,
84"030 W) by comparing relative abundance of species in
each habitat with Hyalella recovered from fish stomachs.
Habitat and fish samples were collected on the same day. In
both lakes, fish were collected by seining in the littoral zone.
Fish in the genus Lepomis, the dominant predators
(Wellborn 1994a), were initially preserved on ice, and their
stomach contents were then preserved in 95% ethanol within
1–2 h of collection. Stomach contents were sorted with the
aid of a dissecting microscope, and recovered Hyalella were
identified to species by the same PCR protocol used for
habitat samples. In Duck Lake, species relative abundance in
the habitat was determined from samples collected for the
spatial distribution study. In South Lake, species relative
abundance in the habitat was assessed by collecting
numerous sweep net samples haphazardly throughout most
of the littoral zone, but not including the very shallow edge
habitat along the shore. These South Lake samples were
pooled, preserved in 95% ethanol, and Hyalella were
recovered from random subsamples with the aid of a dissecting microscope. For South Lake, we measured the head
length of individuals in habitat and fish stomach samples in
order to assess size-biased predation (head length is strongly
correlated with total length and body mass in Hyalella
(Edwards and Cowell 1992; Pickard and Benke 1996).
Within each lake, individual habitat samples were pooled
for fish predation analyses, as were amphipods collected
from fish. We used v2-tests in each lake to evaluate species
differences in relative predation risk. We first examined a
two-way table with abundance of each species crossed with
source (fish stomach, habitat). When this overall analysis was
significant, we then examined all pairwise species combinations, using the Bonferroni procedure to control type I
error. To assess size-biased predation in South Lake, we used
two-factor ANOVA with source and Hyalella species as
factors, and head length as the dependent variable. To
quantify relative predation risk, we used Manly’s preference
index assuming no food depletion (Chesson 1983).
Results
Spatial distribution of species
In Sullivan Lake, relative abundance of the three cryptic
species (Fig. 1) differed among distance-from-shore
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Oecologia (2007) 154:175–183
0.8
Table 2 Two-way ANOVA results for the spatial distribution of
Hyalella species in Duck Lake
A
B
0 .4
C
0.2
<0.5
5
P
1
14.36
0.001
Distance from shore (5, 10 m)
1
1.43
0.24
Depth · distance interaction
1
0.15
0.70
transects (MANOVA, df = 2.46, Wilk’s k = 0.0548,
P < 0.001). Furthermore, univariate tests indicted that each
species’ proportional abundance differed among transects
(Table 1). Species B dominated in the edge habitat, where
it comprised 86% of the Hyalella community, and species
A dominated in the habitat farthest from shore where
it comprised 81% of the community (Fig. 1). Relative
abundance of species was somewhat more equitable at the
intermediate distance from shore, with species A making
up 52% of the community and species C comprising 32%
of the community.
In Duck Lake, only one individual of species B was
collected in habitat samples, and thus only species A and C
were included in analyses. Our primary analysis examined
the relative abundance of Hyalella species at two distances
from shore (5 and 10 m), crossed with two vertical depths
(near surface, mid-depth). In the two-way ANOVA, only
the main effect of vertical depth was significant (Table 2),
with species A comprising a greater proportion of the
Hyalella community in the near-surface habitat than in the
mid-depth habitat (Fig. 2). We performed two secondary
analyses comparing the Hyalella community in two less
common habitats with that of the common habitats. Hyalella relative abundance at the base of the emergent plant,
Table 1 Results of univariate ANOVA analyses of spatial distribution of Hyalella species in Sullivan Lake. edge, 5 m, 10 m Distancefrom-shore transects
Species
df
F
P
Species A
2. 47
29.36
<0.001
Pairwise testsa: edge < 5 m, edge < 10b, 5 m = 10 m
<0.001
Species C
0.006
5.62
Pairwise tests: edge < 5 m, edge < 10, 5 m = 10 m
a
Pairwise tests use Bonferroni-corrected P-values within each
species
Inequality signs (<, >) indicate significant differences
arrowweed, did not differ from that found in either the
near-surface (ANOVA df = 1.16; F = 1.097; P = 0.31) or
mid-depth (ANOVA df = 1.12; F = 1.489; P = 0.25) habitats in the transect 5 m from shore. Hyalella relative
abundance in submerged macrophytes that did not extend
to the surface differed from that found in the near-surface
(ANOVA df = 1.13; F = 54.562; P < 0.001), but not middepth (ANOVA df = 1.16; F = 0.834; P = 0.37) habitats in
the transect 10 m from shore.
Predation risk
In South Lake, 41 bluegill (Lepomis macrochirus) and one
green sunfish (Lepomis cyanellus) were collected, with a
mean size of 88.9 mm (SD = 8.0) total length. Hyalella
were recovered from 76% of fish, with these fish consuming 1–157 individuals (mean ± SD = 39.4 ± 43.5). In
Duck Lake, 54 bluegill and nine pumpkinseed sunfish
(L. gibbosus) were collected, with a mean size of 61.8 mm
(SD = 14.8) total length. Hyalella were recovered from
52% of fish, with these fish consuming 1–12 individuals
(mean ± SD = 4.1 ± 0.9). Although almost all amphipods
in habitat samples were identified to species using PCR,
identification was somewhat less successful for amphipods
recovered from fish stomachs, with 71 and 95% identified
1.0
10 m
t r a n sec t
0.8
0.6
0.4
5m
t r a n s e ct
0.2
Surface
Middepth
Mid-depth,
no canopy
Arrowweed
M i cr o h a b i t a t
Species B
2. 47
49.73
Pairwise tests: edge > 5 m, edge > 10, 5 m = 10 m
2. 47
33
10
Fig. 1 Proportion of community (mean ± SE) for Hyalella species A
(filled circle), B (filled square), and C (filled triangle) across three
distances from shore in Sullivan Lake
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F
Vertical depth (near surface, mid-depth)
Error
Distance from shore (m)
b
df
Effect
0.6
Proportion of community
for species A
Proportionof community
1.0
Fig. 2 Proportion of Hyalella species A (mean ± SE) in microhabitats of Duck Lake. The community was examined in macrophytes
along transects 5 m (filled circle) and 10 m (open circle) from shore,
and microhabitats included two vertical depths [just below the surface
(Surface) and 20–30 cm below the surface (Mid-depth)] in each
transect. Additional microhabitats examined were the base of the
emergent plant ‘‘arrowweed’’ and within macrophytes that did not
extend to the surface (Mid-depth, no canopy)
Oecologia (2007) 154:175–183
179
a
Table 3 Results of contingency table analysis of Hyalella species
abundances from habitat and fish stomach samplesa
2
<0.001
A, B
72.94
1
<0.001
A, C
26.19
1
<0.001
A, B, C
27.70
1
<0.001
A, B, C
B, C
318.81
2
<0.001
A, B
401.68
1
<0.001
A, C
B, C
75.18
136.30
1
1
<0.001
<0.001
0.6
0.4
Relative abundance
66.09
Duck Lake
0. 1
0 .2
0.01
b Duck Lake
1.0
0.6
a
All three species were included in an initial analysis for each lake,
followed by a posteriori pairwise contrasts. All contrasts are significant (all a posteriori contrasts within a lake yield P-values below the
most stringent Bonferroni criterion of P = 0.017)
1 .0
Relative predation risk
P
Species
South Lake
X2
df
Location
South Lake
0.1
0.4
0 .2
in South and Duck Lakes, respectively. Only individuals
identified to species were used in the analysis.
In both Duck and South Lakes, risk of predation differed
among species, and the species order of predation risk was
B > C > A in both lakes (Table 3; Fig. 3). Relative risk of
species B was much greater than that of the other species.
In South Lake, species B constituted 62% of individuals
recovered from fish stomachs, but only 5% of individuals
in habitat samples. Species B had lower relative frequency
in fish stomachs in Duck Lake (13%), but the habitat frequency of Species B was very low (<0.3%), with only one
individual collected in the habitat study. In contrast, species A constituted roughly 40% of the Hyalella community
in habitat samples in both lakes, but was consistently
under-represented (relative to frequency in the habitat) in
fish stomachs. Species C was intermediate between these
extremes, being somewhat under-represented in fish
stomachs in Duck Lake, and somewhat over-represented in
South Lake.
We interpret species differences in relative abundance
between fish stomachs and habitat samples to be caused by
differential predation among species. This interpretation,
however, rests on the assumption that our habitat samples
accurately characterized the species distribution of Hyalella in the habitat. An alternative explanation is that species
differences in our calculation of relative risk could result
from inaccurate assessment of species frequencies in the
habitats. Our results from Sullivan Lake found that species
B was abundant in the narrow edge habitat, and it seems
reasonable to suppose that species B might also be common in the edge habitats of South and Duck Lakes, the
lakes where the fish predation studies were conducted. We
did not include the edge habitat in our habitat samples of
South and Duck Lakes, suggesting that species B was
probably underestimated in habitat samples, and therefore,
0.01
A
B
C
Hyalella species
Fig. 3 Relative abundance of each Hyalella species in fish stomachs
(light bars) and habitat samples (dark bars) in a South Lake and
b Duck Lake. Relative predation risk of species is shown for actual
data (filled diamond with continuous line) and after imposing a
tenfold increase in the habitat abundance of species B (open diamond
with dashed lines)
its relative risk was probably overestimated in our study
(and, consequently, relative risk of other species was
underestimated). To assess the extent of possible bias in
our estimate of relative risk, we explored how our results
change when we impose a tenfold increase in the proportional frequency of species B in the habitat samples. We
examined a tenfold increase in abundance of species B
because this is roughly the magnitude of species B’s
abundance difference observed between the edge environment and other habitats in Sullivan Lake (Fig. 1). In both
lakes, rank order of relative risk among species does not
change, and relative risk of species B remains substantially
greater than that of the other species (Fig. 3). We note that
the tenfold increase in species B in the habitat probably
represents an overestimate of its actual proportional
abundance in the littoral zone as a whole. Assuming the
distribution of species B in Duck and South Lakes is
similar to that observed in Sullivan Lake, then species B is
expected to be abundant only in the narrow edge region
that comprises a very small proportion of the littoral zone
area. If we estimate that the edge habitat extends to 0.5 m
of shore, while the littoral zone extends approximately
15 m from shore, then the edge comprises only about 3%
of the surface area of the littoral zone. Therefore, even if B
is abundant in the edge habitat, its overall abundance in the
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Oecologia (2007) 154:175–183
Table 4 Two-way ANOVA andresults of planned comparisons for
evaluation of size-biased predation on Hyalella species in South Lake
df
Effect
F-ratio
P
Overall analysis
Source (fish, habitat)
1
79.577
<0.001
Species
2
8.062
<0.001
2
1.914
0.148
Source · species interaction
Error
726
Single species analyses of size-biased predation
Species A
Species B
1, 71
1, 338
13.947
25.410
<0.001
<0.001
Species C
1, 317
136.379
<0.001
littoral zone will be small compared to A and C, suggesting
that undersampling of B will have only small effects on
relative risk. We conclude, therefore, that the strong differences in risk observed are unlikely to be simple artifacts
of biases arising from our habitat sampling procedure.
Size-biased predation was evaluated in South Lake. Twofactor ANOVA revealed a significant effect of source (habitat, fish stomach), indicating size-biased fish predation on
Hyalella (Table 4, Fig. 4), and revealed a significant effect of
Hyalella species, indicating that species differed in size. The
interaction term was not significant, suggesting that the form
of size-biased predation was similar among species. ANOVA
analyses of size-biased predation for individual species
showed that, in each species, mean size of individuals consumed by fish was greater than mean size of individuals
collected in the habitat samples (Table 4; Fig. 4).
Discussion
Head length (mm)
We found that three cryptic species of Hyalella amphipods
exhibit substantial differences in both spatial distribution
0.6
0.4
Habitat
Fish
*
*
*
0.2
B
C
A
Hyalella species
Fig. 4 Head length (mean ± SE) of Hyalella species in habitat
samples (dark bars) and fish stomachs (light bars) in South Lake.
Asterisks indicate significant differences (P < 0.05) from ANOVA
123
and predation risk, both of which are common axes of
niche diversity in communities (Organ 1961; Paine 1966;
Brown et al. 1994; Losos 1994; Skelly 1995; Bohanan and
Lenski 1999; Nicholls and Racey 2006). In Sullivan Lake
our analysis focused on species distributions across the
gradient from the very shallow shoreline edge habitat out
to the deep littoral region near the transition to open water.
The Hyalella community changed markedly over this
gradient, and species B and A had strongly complementary
distributions (Fig. 1). Species B dominated in the edge
habitat while species A dominated in the habitat most
distant from shore. At an intermediate distance from shore,
species A and C occurred at roughly similar frequencies,
with species B present at low frequency. In Duck Lake, a
primary focus of our sampling was to assess the vertical
distribution of Hyalella species within macrophytes. We
found a significant shift in species frequencies over the
vertical depth gradient (Fig. 2), with species A and C
occurring at roughly equal frequencies at mid-depths, but
with species A dominating the community near the water
surface. Furthermore, this pattern was consistent across two
transects that differed in their distance from shore. In
contrast to results from Sullivan Lake, species C remained
common at the most distant transect in Duck Lake, at least
in mid-depth samples. Duck Lake also differed from Sullivan Lake in the nearly complete absence of Species B in
habitat samples. In part, the low frequency of species B in
our samples may be the result of our not sampling the
shoreline edge habitat in Duck Lake, but we suspect that
species B has a generally low frequency in the lake because
it was also relatively uncommon in fish stomachs.
The three Hyalella species also differed in predation
risk, and patterns of risk were consistent across the two
lakes examined. Species B had the highest relative risk,
and occurred at a much higher frequency in fish stomachs
than in the habitat samples. These results are consistent
with strongly selective predation on species B. Conversely, species A had a low relative risk in both lakes,
while relative risk of species C was intermediate between
those of the other species. Because species differ somewhat in mean adult body size (Wellborn and Cothran
2004), size-biased predation may contribute to species
differences in predation risk. Indeed, rank orders of both
mean adult body size and relative risk are concordant,
with B > C > A. Furthermore, within each Hyalella species, we found that larger individuals were more susceptible to predation than smaller individuals, a finding
consistent with previous studies of size-biased predation
in Hyalella (Wellborn 1994a). Although the species differ
in mean adult body size, it is not clear that these relatively
small differences in size can fully explain the large disparity in susceptibility to predation. For many aquatic
species, other phenotypic traits, such as differences in
Oecologia (2007) 154:175–183
activity level (Wellborn et al. 1996), contribute to differential risk. Activity level increases with body size in at
least some Hyalella species (Wellborn 1994b), suggesting
that activity level may also play a role in generating
species differences in risk.
Association between observed species differences
and coexistence
In this section we ask what the ecological differences
observed among species may imply about the mechanisms
that maintain diversity in the Hyalella community. Species
within a guild may coexist stably when each species is
more limited by increases in its own density than by that of
other species (Chesson 2000). Coexistence therefore
requires that species differ appropriately in ecologically
relevant traits, with these traits collectively defining species niches (Chase and Leibold 2003). The existence of
ecological differences among species does not, however,
directly imply that species possess the appropriate forms
of niche differentiation required for stable coexistence
(Leibold 1998). Chesson (2000) emphasized that stable
coexistence among species within a guild is promoted by
both equalizing mechanisms that reduce ‘‘fitness differences’’ among species, and stabilizing mechanisms that
will usually be expressed as tradeoffs that cause each
species to be limited more by its own density than by that
of its competitors.
Equalizing mechanisms promote coexistence because
the more similar species are in their per capita response to
relevant ecological factors (niche components), the smaller
the degree of stabilizing niche differentiation required to
coexist stably (Leibold 1998; Chesson 2000). In the sympatric Hyalella community, size-biased predation by Lepomis sunfish may impose a strong equalizing effect by
driving evolution of all species to relatively small body size
(this study, and see Wellborn 1994a; Wellborn et al. 2005),
and thereby preventing large asymmetries in resource
competitive ability (Wellborn 2002). Experimental studies
indicated that Hyalella grazing rates increase with body
size (Wellborn 1994b), and body size is positively associated with competitive ability in species that differ substantially in size (Wellborn 2002). Stabilizing effects
generally result from complementary tradeoffs among
species, with advantages in some aspects of ecological
performance associated with disadvantages in other aspects
(Chesson 2000). These tradeoffs will often be manifest in
ecological studies as complementarity among niche components. In our study, the strongest patterns of complementarity were seen between species A and B, the species
with the smallest and largest mean size, respectively
(Wellborn and Cothran 2004). These species exhibited
181
strong complementarity in habitat distribution in Sullivan
Lake, where both species were common, and they exhibited strong complementarity in predation risk in both lakes
where risk was evaluated.
Although conditions required for stable coexistence in
homogeneous environments have been thoroughly
explored (Tilman 1982), our results suggest these models
are not applicable to the community of cryptic Hyalella
species. The strong spatial structuring of the Hyalella
community in these lakes implies that the littoral zone is
ecologically heterogeneous, and that this spatial heterogeneity is integral to understanding community diversity.
Coexistence in heterogeneous environments has been
examined for two general forms of spatial heterogeneity.
Heterogeneity may be ordered, with changes in the
environment occurring along distinct gradients (Leibold
1996, 1998), or it may occur in the form of more or less
randomly distributed among-patch heterogeneity (Tilman
1982). Our study suggests that heterogeneity in ecological
factors occurs across distance-from-shore and vertical
depth gradients, so we focus on this form of spatial
heterogeneity.
Patterns of complementarity observed in this study,
taken together with previous studies, are most suggestive of
predator-mediated coexistence expressed along habitat
gradients (MacArthur 1972; Vance 1974; Armstrong 1979;
Holt et al. 1994), especially as envisioned in Leibold’s
(1996) model of keystone predation. In this model, species
coexist through competitive ability–predation risk tradeoffs
such that the stronger competitor is more susceptible to
predation, a tradeoff that appears to be common (Mills
et al. 1993; Menge et al. 1994; Werner and McPeek 1994).
The model evaluates coexistence and dominance patterns
across a resource productivity gradient. One prediction
derived from the model is that, at low resource productivity, the species better at exploiting resources is dominant, and at high resource productivity, the species better at
avoiding predation is dominant. At intermediate productivities, two-species stable coexistence is possible (but not
assured), with turnover in composition of coexisting species pairs along the gradient (Leibold 1996). Changes in
dominance or composition of coexisting species across the
littoral zone gradients observed in our study could, therefore, be driven by underlying gradients in resource productivity and predation risk.
As described earlier, a predation risk–competition
tradeoff can be mediated by body size in Hyalella because
any positive effects of stronger competitive ability with
increasing size will likely also entail increased predation
risk (Wellborn 2002). In the sympatric Hyalella community, species A has the smallest mean adult body size and
lowest predation risk, and thus may be a risk-avoidance
specialist, while species B, with the highest risk and largest
123
182
size, may be a competitive-ability specialist. Species C is
intermediate in both size and risk, and may represent a
generalist phenotype that is successful under intermediate
conditions. We do not know how resource productivity
changes across distance-from-shore and vertical depth
gradients, but, based on the keystone predation model
(Leibold 1996), we would predict an increase in productivity with distance from shore and proximity to the water
surface. We are not aware of studies specifically evaluating
periphyton production within macrophytes across these
gradients, but there clearly are vertical and horizontal
gradients in physiochemical parameters within macrophytes (Wetzel 1983; Smiley and Tessier 1998) that may
give rise to productivity gradients. Our study also suggests
that the lake littoral zone may present a gradient of predation risk. For example, foraging ability of fish may be
reduced in the very shallow edge habitat, allowing the
putative competition specialist, species B, to dominate in
the edge habitat.
We argued above that species differences in predation
risk and habitat use are consistent with the kinds of
stabilizing mechanisms that allow stable coexistence in
communities. These ecological differences are not, however, inconsistent with alternative mechanisms that
maintain species diversity. One obvious alternative to
stable coexistence suggested by our results is that diversity is maintained through source-sink dynamics within
a heterogeneous landscape (Shmida and Elner 1984;
Amarasekare and Nisbet 2001; Mouquet and Loreau
2003). Each species may be dominant within a limited
region of the littoral zone, such that it would ultimately
exclude other species in the absence of immigration to
that region of the habitat. Shifts in dominance across an
ecological gradient require only small differences among
species in traits that shape species responses to the environmental factor that changes along the gradient (Leibold
1998). In this metacommunity perspective, diversity in
any region of the littoral zone is maintained by continual
dispersal dynamics of species into sink regions (Amarasekare and Nisbet 2001). In Sullivan Lake, for example,
our observational study is consistent with competitive
dominance shifting from species B in the edge habitat, to
species C in the middle region of the littoral zone, to
species A farther from shore. In the absence of experimental data, one could postulate, in fact, that maintenance
of diversity via sequential dominance coupled with dispersal is a more parsimonious hypothesis than stable
coexistence because competitive dominance does not
require the kinds of restrictive balancing of equalizing
and stabilizing effects necessary for stable coexistence
[see, for example, discussion of tradeoffs among zero net
growth isoclines and impact vectors required for coexistence in Leibold (1998)].
123
Oecologia (2007) 154:175–183
Conclusion
The explosive growth of genetic studies documenting
cryptic species diversity (Gomez et al. 2002; Hebert et al.
2004; Molbo et al. 2003; Hogg et al. 2006; Stuart et al.
2006) makes clear that communities are more species rich
than we had imagined. Co-occurrence of species with high
phenotypic similarity is a reality (Muller 2000; Gomez
et al. 2002; Molbo et al. 2003; Matthews 2006; Nicholls
and Racey 2006), but it remains to be seen whether traditional models can explain persistence of multiple cryptic
species in a community (McPeek and Gomulkowicz 2005;
Leibold and McPeek 2006). Our study and at least one
other recent study of cryptic species (Nicholls and Racey
2006), suggest that species with high phenotypic similarity
can differ strongly in ecologically important ways, suggesting that traditional niche partitioning mechanisms may
be sufficient in at least some communities. These findings
may simply suggest that morphological and ecological
similarity are sometimes not intimately coupled, and we
should abandon our bias of viewing coexistence through a
lens of ‘‘limiting similarity’’ (Leibold 1998). If subtle trait
differences engender large ecological differences, then
coexistence of cryptic species offers no special challenge to
traditional models of coexistence. In some communities of
phenotypically similar species, however, it seems unlikely
that species co-occurrence is achieved through niche-based
stable coexistence, and non-equilibrium and metacommunity perspectives are likely to be more fruitful (McPeek and
Gomulkowicz 2005; Leibold and McPeek 2006). Elucidation of the ecological dynamics that maintain diversity in
communities of cryptic species must await experimental
tests that differentiate among alternative mechanisms, and
such studies may well broaden our view of the variety of
processes that maintain biological diversity.
Acknowledgements We thank Christine Relyea for help with field
collections. The manuscript was improved by insightful comments
from John White, Dan Allen, Puni Jeyasingh, and Matt Chumchal.
Our work was supported by the National Science Foundation.
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