Overdispersion of body size in Australian desert lizard communities at local scales only: no evidence for the Narcissus effect
- First Online:
- Cite this article as:
- Rabosky, D.L., Reid, J., Cowan, M.A. et al. Oecologia (2007) 154: 561. doi:10.1007/s00442-007-0849-1
- 195 Views
Both local and regional processes may contribute to community diversity and structure at local scales. Although many studies have investigated patterns of local or regional community structure, few have addressed the extent to which local community structure influences patterns within regional species pools. Here we investigate the role of body size in community assembly at local and regional scales in Ctenotus lizards from arid Australia. Ctenotus has long been noted for its exceptional species diversity in the Australian arid-zone, and previous studies have attempted to elucidate the processes underlying species coexistence within communities of these lizards. However, no consensus has emerged on the role of interspecific competition in the assembly and maintenance of Ctenotus communities. We studied Ctenotus communities at several hundred sites in the arid interior of Australia to test the hypothesis that body sizes within local and regional Ctenotus assemblages should be overdispersed relative to null models of community assembly, and we explored the relationship between body size dispersion at local and regional scales. Results indicate a striking pattern of community-wide overdispersion of body size at local scales, as measured by the variance in size ratios among co-occurring species. However, we find no evidence for body size overdispersion within regional species pools, suggesting a lack of correspondence between processes influencing the distribution of species phenotypes at local and regional scales. We suggest that size ratio constancy in Ctenotus communities may have resulted from contemporary ecological interactions among species or ecological character displacement, and we discuss alternative explanations for the observed patterns.
KeywordsCharacter displacementCommunity assemblyCompetitionNull modelRegional diversity
Despite several decades of study, the processes influencing the assembly of ecological communities at local and regional scales remain a subject of considerable debate (Brown et al. 2000; Stone et al. 2000; Morena 2006). At local scales, niche differences among species have long been assumed to play a central role in community assembly because competitive exclusion and ecological character displacement can result from interspecific competition for shared resources (MacArthur and Levins 1967; Schluter 2000). The view that niche differences can promote species coexistence by reducing the intensity of interspecific competition is supported by theoretical and experimental results (MacArthur and Levins 1967; Schoener 1983a) and by patterns of trait overdispersion within communities, whereby traits related to resource use show greater dispersion among co-occurring species than expected in the absence of interspecific competition (Case and Sidell 1983; Schoener 1983b; Gotelli and Graves 1996).
Despite a large and growing body of literature on community-wide trait overdispersion (Dayan and Simberloff 2005), few studies have simultaneously considered the processes influencing community assembly at both local and regional scales (Stone et al. 2000). This is an important issue because the interpretation of patterns within local communities may be conditional upon patterns within the larger regional species pools from which local communities are drawn. For example, many studies have contrasted the dispersion of morphological or ecological traits within local communities to those of communities drawn randomly from the regional species pool (e.g. Fox and Brown 1993; Nipperess and Beattie 2004). Colwell and Winkler (1984) noted that such studies might underestimate the intensity of interspecific competition if the distribution of traits within regional species pools has already been influenced by competition. This phenomenon, termed the Narcissus effect, can occur if interspecific competition has caused the regional elimination of species most susceptible to competition.
To date, evidence for the Narcissus effect has been controversial. Brown et al. (2000) contend that regional assemblages of North American desert rodents have been shaped by competition. Stone et al. (2000) claim that little evidence exists for such structure at the level of the regional species pool that cannot be explained by the geography of speciation, differential dispersal abilities or other processes. They further suggest that only Bowers and Brown’s (1982) work on body mass in regional and local assemblages of heteromyid rodents supports the view that local processes can result in structured regional assemblages. Other studies employing detailed analyses of trait or functional group dispersion at local and regional scales have failed to reach consensus on this issue. For example, Nipperess and Beattie (2004) found evidence for morphological overdispersion of regional pools in arid Australian ant communities, but Gotelli and Ellison (2002) found that body sizes in North American ant communities were random or weakly clustered at regional scales.
Here we test for overdispersion of body size at local and regional scales in communities of Ctenotus lizards from arid Australia. With nearly 100 described species, Ctenotus is Australia’s most diverse terrestrial vertebrate genus. Ctenotus occurs in virtually all habitats in Australia, but the majority of species inhabit the arid and semi-arid regions of the continent, with diversity peaking in the western arid interior (Pianka 1981; James and Shine 2000). Body size in Ctenotus appears to be correlated with variation along several major niche axes, including prey size and microhabitat (Pianka 1969b, 1986; James 1991; Garland and Losos 1994), suggesting that size may be a useful summary of niche use in several dimensions. Although Ctenotus has served as a model system for understanding species richness and coexistence, there is no consensus on the significance of divergence along these or other resource axes for the assembly and maintenance of Ctenotus communities (Pianka 1989, 1969b; Morton and James 1988; James 1991; James and Shine 2000).
Because Ctenotus body size is putatively associated with niche use, overdispersion of body size at the local or regional scale may reflect interspecific competition or ecological character displacement. We use data drawn from several hundred Ctenotus communities within seven regional species pools to address two principal objectives. We test the hypothesis that body sizes within local Ctenotus assemblages should be overdispersed relative to those expected under null models specifying an absence of deterministic effects on body size. In addition, we evaluate evidence for a Narcissus effect by testing whether regional species pools are themselves overdispersed, and we investigate the relationship between the magnitude of overdispersion at local and regional scales.
Materials and methods
Body size estimation
This is equivalent to representing each data point Xi by a normal distribution with μi = Xi and with a common variance h2 for all data points. The density estimate p(k) is simply the summed densities of all points in X taken at point k. The standard deviation h of the smoothing kernel, also known as the bandwidth, controls the shape of the estimated density function. If h2 is too large, the estimated density p(k) will approach a uniform distribution; if it is too small, a mode will occur at every data point. We used the default bandwidth selection algorithm in “density”, which follows guidelines in Silverman (1986); density estimates were visually compared to histograms of the raw data to ensure that this procedure resulted in the appropriate choice of bandwidth.
The upper mode of the estimated density function was used as our index of adult body size (Fig. 2). Because body size in Ctenotus can vary geographically and because our datasets span a vast portion of interior Australia, we estimated region-specific sizes for species. Due to the close geographic proximity of datasets U1 and U2 (Uluru National Park) and of datasets L1 and L2 (Lorna Glen Station), we estimated body sizes from pooled capture data within each of these regions. We did not distinguish among male and female lizards because Ctenotus species show low levels of sexual size dimorphism (Pianka 1969b) and because they are often difficult to sex accurately in the field (Read 1998). Estimates of SVL for all species, as well as numbers of measured lizards per dataset, can be found in Electronic Supplementary Material S2.
Analysis of size overdispersion
Log-uniform model: Under the log-uniform model (LU), random assemblages were generated by sampling from a log-uniform distribution on the interval defined by the largest and smallest species occurring in a particular regional assemblage. A single iteration of the process for the ith site in the kth regional assemblage proceeded as follows. If N species occurred in region k, the endpoints of the distribution were fixed at the largest (max) and smallest (min) species observed in k. Two species were assigned observed min and max values, and body sizes for the remaining N − 2 species were sampled from a log–uniform distribution bounded by these min and max values. If ni species occurred at site i, ni body sizes were chosen from this source pool of N random body sizes in assemblage k.
Log-normal model: Under the log–normal (LN) model, body sizes for each site were drawn from a log–normal distribution with the same mean and variance as the observed distribution of body size for each region. As for the LU model, we chose exactly ni random body sizes for each site with ni species present.
Pool model: In this model, we compared observed assemblages to all possible combinations of the same species richness from the regional source pool (Schoener 1983b). Thus, body sizes at each site were constrained to those found in a particular region.
These three null models differ in the assumptions they make about the evolutionary and ecological processes underlying the distribution of size ratios in local communities. The LU null model assumes that all body sizes are possible within the morphospace defined by the largest and smallest species in the regional dataset, and the LN model assumes that body sizes follow a log–normal distribution. In contrast, the pool model assumes that the only possible body sizes at a given site are those already present in the regional species pool. If regional species pools are morphologically overdispersed, local communities drawn randomly with respect to body size from the regional pool will generally be overdispersed under LN and LU models, but not under the pool model.
We repeated our analyses under the LU and LN models for each of the seven regional assemblages. We did not apply the pool model at the regional scale as many species were common to more than one region and because we used region-specific estimates of body size. As for the local scale, we used one-tailed t tests to test the hypothesis that SES values for regions should be less than zero.
If Ctenotus communities are characterized by a Narcissus effect, it should be most difficult to detect overdispersion of body size at the local scale when regional species pools already show evidence of size ratio constancy. Thus, a local assemblage might show no evidence for body size overdispersion relative to a community drawn randomly from the regional pool, if the regional pool is already morphologically overdispersed. We predicted that a Narcissus effect would result in an inverse correlation between the intensity of overdispersion at regional and local scales: as the intensity of regional-scale overdispersion increases, we expect a corresponding decrease in the intensity of local-scale overdispersion, at least under the pool null model. We tested this prediction by examining the correlation between regional effect sizes (SES) and the mean SES for sites within regions.
Because arid zone Ctenotus communities vary considerably among habitats (Pianka 1986), we sought to determine the extent to which patterns observed across all sites differed among major habitat associations. We classified sites based on the abundance of spinifex grass (Triodia spp.), which is perhaps the single-most important habitat variable influencing Ctenotus community composition and diversity at local scales (Pianka 1986; Morton and James 1988; James and Shine 2000). Spinifex is a dense, prickly form of vegetation that can be exceedingly abundant in the western and central regions of the arid interior. It may provide lizards with protection from predators, favorable microclimates and an abundance of termites and other arthropod prey (Pianka 1981, 1986; Morton and James 1988); for these reasons, spinifex has been hypothesized to play a central role in promoting high species diversity in Australian desert lizard communities (Morton and James 1988; Pianka 1989). Our habitat categorization was based on a simple qualitative assessment of whether spinifex constituted the dominant form of vegetation at each site; we then tested for significant differences in SES values among these two habitat categories using two-sample t tests.
Meta-analysis of the dispersion of body size across sites in nine datasets as measured by the variance in size ratios within local assemblages of Ctenotus lizards from arid Australia
Because our nine datasets came from seven regions (U1 and U2 from Uluru National Park, and L1 and L2 from Lorna Glen Station), it could be argued that these datasets cannot be treated independently, and that we should have performed t tests only on sites within each region. To address this concern, we created pooled Uluru and Lorna Glen species-by-site matrices and repeated our analyses on the seven regional datasets. Results using these pooled datasets were virtually identical to those presented in Table 1 (combined, Bonferroni-adjusted P values: LN model P < 0.001; LU model P < 0.001; pool model P = 0.040).
Analysis of size-ratio dispersion at the level of the regional species pool
Body size dispersion at local and regional scales
Our results indicate that Ctenotus assemblages in arid Australia are characterized by community-wide overdispersion of body size at local scales (Table 1). Using data drawn from nine independent surveys and multiple sites within seven regional species pools, we found that the variance in size ratios among co-occurring species is less than expected relative to three different null models. To the extent that body size is functionally related to resource use in Ctenotus, our results are consistent with a role for interspecific competition in generating size-structured local assemblages over ecological or evolutionary timescales. We consider alternative explanations for this pronounced overdispersion effect in more detail below.
Two findings would support the operation of a Narcissus effect across the spatial and taxonomic scales considered in this study. First, we would expect to observe little evidence for trait overdispersion at the local scale relative to the “pool” null model, whereby communities are drawn randomly from the regional species pool. Second, we should find evidence that regional species pools are trending towards trait overdispersion. Because the Narcissus effect represents an underestimate of the role of competition inferred under “pool” null models caused by sampling a postcompetition regional species pool (Colwell and Winkler 1984; Stone et al. 2000), we further predicted that regional species pools trending towards morphological overdispersion would show reduced evidence for size ratio constancy at the local scale under the pool null model. This reduction in the magnitude of trait overdispersion was predicted because the distribution of phenotypes within regional pools would already have been shaped by species interactions.
Our results are inconsistent with a Narcissus effect. Although observed effect sizes at the local scale were greater under the continuous distribution null models (LU and LN), we nonetheless observed significant size ratio constancy under the pool model (Table 1). Furthermore, we found no evidence that regional species pools are trending towards overdispersion of body size (Table 2). Finally, there is no relationship between regional scale dispersion of body size and body size dispersion at the local scale under the pool model (Fig. 4).
When we classified sites based on the abundance of spinifex, we found no significant differences in VAR between sites with and without spinifex cover (Fig. 5b), and effect sizes are comparable to those observed for all sites considered together (Table 1). We appreciate that this simple binary habitat classification fails to recognize many plant and substrate associations within the Australian arid-zone. For example, the spinifex category included sites characterized by many different canopy species occurring over a range of substrates, including sandplain with Eucalyptus gongylocarpa overstory, Thryptomene-dominated dune and swale and rubble-strewn erosional surfaces. Nonetheless, spinifex is clearly one of the most important habitat variables influencing Ctenotus community composition (Fig. 5a; Pianka 1969a, 1972), and our results suggest that size ratio constancy within Ctenotus communities is not driven by patterns associated with a single widespread habitat.
Evolutionary and ecological causes of size ratio constancy
The tendency towards size ratio constancy suggests that the distribution of Ctenotus phenotypes in local communities has been influenced by interspecific competition. Trait overdispersion can be caused by competitive exclusion occurring over ecological timescales or by character displacement (Case and Sidell 1983; Dayan and Simberloff 2005). Although we cannot rigorously demonstrate character displacement without incorporating additional phylogenetic information (Losos 1990), we note that body size is one of the principal phenotypic axes along which character displacement has been observed in lizards (Giannasi et al. 2000; Radtkey et al. 1997; Melville 2002).
Interspecific competition can influence trait distributions within communities by favoring phenotypes that exploit under-utilized resources, or through behavioral interference among individuals with similar phenotypes. The latter, typically referred to as interference competition, is an alternative to the more commonly considered interactions involved in direct interspecific resource competition (Case and Gilpin 1974; Adams 2004). Interference competition is particularly likely if the intensity of behavioral interference is proportional to the extent to which individuals overlap in body size (e.g. Palomares and Caro 1999). Consistent with the possibility of interference competition, we note that body size plays a critical role in mediating interspecific aggression in some lizards (Losos 1996; Melville 2002) and in a number of other taxa (Alatalo and Moreno 1987; Robertson 1996).
Such behavioral interactions do not rule out resource competition as a causal process, because size-conditional behavioral interference could reflect an evolutionary response to potential resource competitors. Resource competition has been implicated as a primary cause of interspecific aggression (Polis et al. 1989), and in some taxa, the intensity of interspecific aggression is related to dietary overlap (Donadio and Buskirk 2006). Melville (2002) attributed character displacement in several species of Tasmanian lizards to interference competition for basking sites, a limiting resource in the alpine habitats where these species occur. Considerable theoretical and empirical evidence now supports the view that interference competition can result in character displacement (reviewed in Dayan and Simberloff 2005), although recent work on carnivores suggests that some types of interference competition may actually favor convergence in body size (Donadio and Buskirk 2006). The relationship between interference and resource competition deserves further study in Ctenotus and other systems.
Alternative explanations for size ratio constancy that do not require a role for interspecific competition include non-random distributions of resources (Schluter and Grant 1984), predation (Jeffries and Lawton 1984) and reproductive character displacement (Pfennig and Pfennig 2005). Although overdispersion of Ctenotus phenotypes may be attributable to prey size or microhabitat features, characterizing differential resource availability in such complex, multidimensional systems poses a daunting challenge. There is no obvious multimodal signal in the distribution of prey sizes taken by Ctenotus (Pianka 1969b), possibly due to the large numbers of termites consumed by all species. However, it is possible that discontinuities exist along other resource axes or in prey size during periods of severe resource limitation. In one of the most thorough analyses of resource partitioning in Ctenotus, James (1991) found that five syntopic Ctenotus species partitioned termite prey by generic or functional-group identity, but not by size, during the driest year of his study.
It is difficult to assess the effects of selective predation on the distribution of body size in Ctenotus, but we note that Ctenotus predators include a variety of generalists, including several species of varanid lizards, elapid snakes and the pygopodid Lialis burtonis (Patchell and Shine 1986). Varanid lizards, for example, are a principal Ctenotus predator in Australian deserts, and dietary analyses indicate that they opportunistically prey upon virtually all species of Ctenotus that they encounter (Pianka 1994). As virtually nothing is known regarding mate choice in Ctenotus, we can at best acknowledge the possibility that reproductive character displacement in size might have contributed to the observed patterns.
If ecological character displacement underlies patterns of size ratio constancy within local Ctenotus communities, why would we have failed to observe overdispersion at the regional scale? One possible explanation is that trait overdispersion in Ctenotus at the local scale may be attributable to evolutionary shifts in habitat among similar-sized species. If the intensity of competition is related to body size overlap, natural selection might favor different patterns of habitat use, rather than evolutionary shifts in body size. Such similar-sized species would thus be retained in the regional species pool, and the regional pool would show little evidence for size ratio constancy. However, at the local scale, we would observe reduced co-occurrence among similar-sized congeners. Because our local communities were defined precisely to capture within-habitat patterns of co-occurrence, we consider this hypothesis to be worthy of future study.
Among terrestrial vertebrates, regional-scale trait overdispersion has been widely reported in communities of carnivorous and granivorous mammals (Dayan et al. 1989; Yom-Tov 1991; Dayan and Simberloff 1994; Kieser 1995; Ben-Moshe et al. 2001). Our large-scale surveys of arid Australian Ctenotus communities reveal a different view of community organization. Although Ctenotus communities are characterized by size ratio constancy at local, within-habitat spatial scales, we find little evidence that local processes in this system “feed up” (Brown et al. 2000) to influence the distribution of body size in regional species pools. Previous research has suggested that species richness at local scales in this system is primarily determined by processes occurring at the regional scale (James and Shine 2000), but our results do not support a similar relationship underlying the distribution of species phenotypes in local and regional assemblages.
We thank D. Adams, A. Agrawal, M. Austin, H. Greene, L. Joseph, I. Lovette, A. McCune, and S. Morton for comments on the manuscript and/or valuable discussion of these topics. For assistance with survey design and other logistics, we thank S. Argus, G. Armstrong, L. Baker, P. Doughty, S. Eldridge, E. Foster, N. Gambold, M. Gillam, J. Gillen, M. Hutchinson, the late K. Jones, I. Kealley, K. Kenneally, A. Kerle, S. Morton, N. de Preu, and D. Stefoni. In addition, we thank the many individuals who assisted with other aspects of this project, including G. Allen, J. Alley, JM Armstrong, M. Barritt, B. Barton, K. Bellchambers, A. Brook, R. Burton, S. Campbell, D. Carter, V. Clarke, J. Cole, J. Coulter, M. Coulter, A. Duguid, M. Fleming, B. Gardiner, K. George, D. Gibson, D. Graham, A. Grattidge, Greenie, G. Hearle, R. How, J. and J. Kavanagh, D. Langford, B. Lewis, R. Lynch, C. Martin, D. Mason, G. McKenzie, J. Patten, N. Rabillier, A. Richardson, D. Risby, B. Ryan, D. Schunke, P. Spencer, L. Stokes, P-J. Waddell, A. Willson, A. Woosnam, and Conservation Volunteers Australia. We also thank the traditional owners from Willowra, Yuendemu and Mutitjulu for allowing us to conduct field work at the Lander River, Sangsters Bore and Uluru Kata Tjuta National Park sites, respectively. Funding for this study was provided by NSF-OSIE- 0612855, an EAPSI Fellowship to DLR, administered jointly by the U.S. National Science Foundation and the Australian Academy of Science, and by Sigma Xi, the Evolutionary Biology Program at the Cornell University Lab of Ornithology, the Mario C. Einaudi Center for International Studies, the Goldfields and LANDSCOPE branches of the Western Australia Dept. for Environment and Conservation, and the Australian National Heritage Trust. Research conducted for this study conforms to current Australian law in every respect.