Foraging guild structure and niche characteristics of waterbirds in an epicontinental lake in Mexico

Bird communities that inhabit aquatic environments usually have a complex structure driven by the large number of variables that influence species interactions (Winemiller and Pianka 1990; Weller 1999; Palmer et al. 2003). Thus far, approaches generally used to understand processes organizing waterbird communities have focused on analyzing patterns of resource partitioning (Schoener 1974; Wiens 1977; Pianka 1980; Winemiller and Pianka 1990; López de Casenave et al. 2008). Research generally concluded that species with similar patterns of resource utilization (i.e., species of the same guild) are susceptible to competitive interactions that affect the community structure.

Patterns of resource utilization (either food or habitat resources) are usually analyzed in the framework of niche theory, i.e., members of the same guild similarly exploit similar resources and may be potential competitors (Root 1967; Albrecht and Gotelli 2001; Palmer et al. 2003). Thus, species of the same guild are susceptible to competitive interactions over shared resources, and in order to coexist, they should show some mechanism to reduce, but not necessarily eliminate, negative competitive interactions (Cody 1974; Simberloff and Dayan 1991).

Most studies searching for patterns of resource utilization evaluated niche breadth and niche overlap. Spatial models of niches were formalized by Hutchinson (1959) who defined niche breadth as the distance through a niche along some particular line in the niche space. In terms of particular resources, niche breadth is the range of resources used by species. Niche overlap refers to the joint use of resources by two or more species (Colwell and Futuyma 1971). Both niche breadth and niche overlap provide indirect ways to explore ecological processes such as competition over shared resources (MacNally 1983).

Schoener (1974) suggested three niche dimensions where species tend to segregate to minimize niche overlap: habitat, food type, and time of habitat occupancy. Thus, characterization of guilds through these dimensions provides information about possible interactions caused by inter- and intraspecific resource partitioning. Studies of waterbird communities have primarily focused on two of the three niche dimensions proposed by Schoener, namely habitat use and food type (Pöysä 1983; Zárate-Ovando et al. 2008; Gatto et al. 2008; López de Casenave et al. 2008), and assume that these two dimensions together suggest resource differentiation (Wiens 1989) and that both dimensions have an effect on the distribution, abundance, and species richness in wetlands (Weller 1999).

Therefore, Robinson and Holmes (1982) proposed an analogy between feeding technique (feeding behavior) and food consumed which was applied in several studies to explain the guild structure and resource partitioning of waterbird communities (Pöysä 1983; Sarrías et al. 1996; Gatto et al. 2008). The advantage of this method is that no dietary study is required for the analysis.

Whether the pattern of resource utilization detected arises from an ecological process, such as competition, is unclear until a comparative study of patterns is carried out to understand processes that underlie the community structure (MacNally 1983; Bell 2001). Under the classical niche paradigm, i.e., competitive niche differentiation resulting from exploitation of limited resources, interspecific competition over shared resources will drive the community structure (MacNally 1983; Hubbell 2006). Alternatively, neutral theory states that patterns can be the result of neutral processes such as stochasticity and dispersal ability rather than competition and niche partitioning (Bell 2001; Hubbell 2001, Hubbell 2006). Where competition results in characteristic ecological patterns, the comparative study of patterns with appropriate neutral models (null models) may reveal the degree of influence of competition on the community structure (Connor and Simberloff 1979; Strong et al. 1979; MacNally 1983; Bell 2001).

The null model is  a pattern-generating model that is based on randomization of ecological data or random sampling from a known or imagined distribution’ (Gotelli and Graves 1996). The null model tests if observed data are non-random with respect to the null hypothesis (Gotelli 2001). Thus, in the context of niche overlap and competition, null modeling allows determination of how much niche overlap could be expected in the absence of competition.

In Mexico, studies of waterbird communities are insufficient and were mostly conducted in coastal wetlands, particularly in the northwestern portion of the country. Those studies analyzed diversity, habitat use, guild structure, and migratory species (see Mellink 2005). However, studies focused on waterbird assemblies in epicontinental lakes are scarce (Ramírez-Bastida 2000; Pineda-López and Arellano-Sanaphre 2010) and largely focused on a single species (Sartor 1989; Munguía et al. 2005; Mellink and Riojas-López 2009; Luevano et al. 2010; Villamagna et al. 2010). Additionally, studies on the community structure of waterbird communities are almost non-existent (see Hernández-Vázquez 2005), and the only study that tested patterns of resource utilization with null models failed in its interpretation (Núñez et al. 2008). Additional studies of waterbirds are needed.

In this study, we evaluated guild patterns of resource utilization within waterbird communities in an epicontinental lake in central Mexico. Three niche dimensions or axes were documented: habitat use, feeding technique, and time. To assess the statistical significance of the observed patterns, we compared observed patterns to those expected under the null hypothesis. Additionally, we discuss ecological mechanisms that structure the waterbird community.

Our study describes the guild structure of a waterbird community in central Mexico and analyzes resource utilization patterns through three niche dimensions: habitat use, feeding technique, and time. Patterns characterized from niche breadth and niche overlap of species showed that species were specialists in feeding technique and more flexible in terms of feeding habitat. To detect if the observed pattern arose from competition between species, null models were used. Niche overlaps of the waterbird community were higher than expected in a community without competition, suggesting a lack of competition. Processes such as morphological differences, different abundances of species, migration, resource fluctuations, and clumped resources could explain the observed patterns.

The bidimensional niche (under the assumption that it reflects differences in resource exploitation; sensu Holmes and Recher 1986) structured the waterbird community into four feeding guilds (Wiens 1989; Sarrías et al. 1996). However, species belonging to the same guild mostly differed in bill and leg morphologies. For instance, guild G2 could be subdivided into subgroups according to morphological characteristics, such as bill or leg size. Morphological differences may explain why members of the same guild feed in different areas using the same techniques or in the same area (apparently exploiting the same resource) but catching different prey (Schoener 1974; Simberloff and Boecklen 1981; Gotelli and Ellison 2002; Zeffer et al. 2003). To provide an accurate description of feeding guilds, more dimensions should be added to the analysis. Data on diet (stomach contents) and availability of prey would be informative (Sarrías et al. 1996).

Important patterns in the waterbird community structure at Lake Acuitlapilco were characterized through niche breadths and niche overlaps. The calculated niche breadths were narrow, suggesting that guilds were mainly specialists in feeding techniques. Only three species (F. americana, A. clypeata, and A. crecca) showed niche breadths wider than the other species. The first two were the most abundant species in the community (Fonseca et al. 2012) and also had the largest values of niche breadth. These species appeared to be unaffected by high abundances of individuals of the same species (A. clypeata) or by changes in food habitat availability (F. americana). The flocking feeding behavior of A. clypeata and F. americana and the wide niche breadths in all dimensions suggest that competition for resources or interspecific competition did not play a major role in structuring their populations.

Additionally, narrow niches suggest that changes in resource availability may also affect the composition of the community (Pöysä 1983). Under this scenario, a fluctuation in resources (habitat) would affect species with a narrow niche breadth, such as wading species (of the Scolopacidae and Charadriidae) from guild G2. These guilds use pecking to opportunistically exploit resources in areas with particular characteristics such as muddy areas and shallow water (Skagen and Knopf 1994). Their presence and abundance were restricted to months of water withdrawal (Pérez-Crespo et al. 2013). In contrast, guilds G4 (A. acuta, A. discors, A. clypeata, A. crecca, and A. platyrhynchos) and G3 (A. cyanoptera, F. americana, G. galeata, L. pipixcan, and P. tricolor) had wider niche breadths in both dimensions and would have been less affected. The ability of these guilds to exploit resources in several habitats of the lake using diverse techniques allowed segregation, thus decreasing potential inter- and intraspecific interactions.

The general pattern of niche overlap found in the Acuitlapilco waterbird community was larger among species of the same guild than between other species in the community. Several authors suggested that competitive interactions are more likely among species of the same guild (Pianka 1980; MacNally 1983; Jaksic and Medel 1990), and they usually occur in guilds with a moderate to small number of species (MacNally 1983). Liordos (2010) found a similar pattern of niche overlap of foraging guilds of waterbirds wintering in a Mediterranean coastal wetland. He concluded that a small niche overlap between species of different guilds suggested a relatively high degree of specialization within the waterbird assemblage. Overlaps of species of the same guild were high, but habitat partitioning was observed. No conclusions about the existence of ecological processes underlying the pattern observed were provided by Liordos. In contrast, the use of null models in our study allowed us to discriminate between ecological phenomena such as competition and species sharing niches.

Results from the null models showed that the observed overlaps were higher than expected, particularly in habitat use and both dimensions together. When data were seasonally subdivided, the same pattern was observed. Therefore, species share habitat more than randomly expected, thus denoting a lack of competition (Gotelli and Graves 1996). Several mechanisms could explain this pattern.

First, seasonal variability of resources allows the addition or removal of species in each guild, reducing competitive interactions (Wiens 1977). Second, clumped resources attract more species and individuals. Studies suggested that shallow waters have greater organic matter and submerged plant beds, providing a rich foraging habitat and protection from predators (Rozas and Odum 1988; Minello et al. 1994; Rozas and Zimmerman 2000; Castellanos and Rozas 2001; Gossman 2005; Cannaday 2006). Other studies also suggested that shallow waters can accommodate more species than deep waters (Williams 1996; Colwell and Taft 2000), which suggests that clumped and rich resources in shallow waters increase bird density there and reduce competition. Third, rather than simply forming in areas of existing high prey density, social flocks may actively enhance their foraging success through herding or confusing escape reactions of prey (Saino et al. 1995; Battley et al. 2003). Guild G2, pickers in water, mud, and vegetation (egrets, ibises, and shorebirds), feed in groups in shallow waters with high prey availability, and aggressive interactions were not noted between individuals when foraging at our study site. Fourth, the existence of differences in morphology between members of the same guild, as mentioned above (Wiens 1989), allows species to coexist. Fifth, the arrival of migrating species in winter coincides with an increased availability of resources and habitats (Aguilar 2003). Finally, differences in species abundances could be a mechanism explaining coexistence. For example, O. jamaicensis (5,300 records, Fonseca et al. 2012) and P. nigricollis (280 records) had almost total niche overlap (all dimensions) and narrow niche breadths. In contrast, A. clypeata and A. platyrhynchos had high niche overlap, but niche breadths and abundances were not equal. Asymmetries in abundance and niche breadth could potentially be acting as mechanisms for coexistence.

In short, our results showed that waterbird species in Lake Acuitlapilco were specialists in resource utilization patterns and therefore vulnerable to fluctuations in resources, particularly feeding habitats. Niche overlaps were generally largest among species belonging to the same guild. The use of null models showed that habitat and observed bidimensional overlaps were higher than those of randomly generated communities, suggesting a lack of competition or species sharing niches. Thus, our study suggested that other processes can be used to predict resource utilization patterns instead of competition alone, as suggested by neutral theory (Hubbell 2001). Future studies analyzing the mechanisms that structure waterbird communities should include the use of null models to support their conclusions.