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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 123 176 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 123 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 177 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 123 178 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 123 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 123 180 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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