Topological analysis of the ecological importance of elasmobranch fishes: A food web study on the Gulf of Tortugas, Colombia

Abstract

We built a trophic network based on a matrix of interspecific trophic relationships to assess the role of elasmobranch fishes in shaping community structure of the Gulf of Tortugas in the Colombian Pacific Ocean. We analyzed diet similarities to define trophic components (nodes) – rather than taxonomical groups – in the network. We evaluated the ecological function of species or trophic entities through topological analysis of their structural importance in trophic networks by applying one local and several mesoscale network indices. We found that top predatory elasmobranchs play an important ecological role in top-down control and in propagating indirect effects through the system owing to high values of the node degree, centrality and topological importance indices. However, invertebrates and teleost fishes had higher connectivity and topological importance than other elasmobranchs in the network before and after removal of top predators from the system. Results from our study thus suggest that elasmobranchs at intermediate trophic levels – commonly referred to as “mesopredators” – are not so important in all complex coastal ecosystems as previously reported.

Introduction

A central theme in the study of trophic networks is how interspecific relationships affect ecosystem dynamics and stability (Pimm, 2002, De Ruiter et al., 2005). The importance of these interactions has given rise to the development of concepts such as multispecies management (May et al., 1979, Yodzis, 2000) or system perspective (Grant et al., 1997), which recognize the need to understand the interactions of not only one species, but of most or all species to model more accurate responses to the dynamics of each system under study (Jordán et al., 2006).

Despite the supposed importance of elasmobranchs in marine trophic network interactions (Stevens et al., 2000, Wetherbee and Cortés, 2004), there are very few studies that have assessed the effect of elasmobranch predation on populations of their prey (direct effects), with a few exceptions that have examined interactions with marine mammals. For example, Lucas and Stobo (2000) and Bowen et al. (2003) suggested that sharks played an important role in the decline of sea lions in Sable Island, and McCosker (1985) proposed a top-down effect of sharks on pinnipeds. García-Gómez (2000) suggested that top shark species are important density regulators because when their biomass decreases that of some of their prey increases significantly.

It has been proposed that ray predation can have a strong impact on benthic prey (Thrush et al., 1994, Myers et al., 2007), to the extent of creating population sinks in specific locations (Peterson et al., 2001). Behaviorally mediated indirect interactions between elasmobranch fishes and their prey have also been suggested as mechanisms to understand community dynamics, whereby the presence or absence of elasmobranch predators condition the behavior and habitat use of their prey (“risk effect”; Heithaus and Dill, 2002, Dill et al., 2003, Heithaus et al., 2008).

Some approaches to understanding the ecological role of elasmobranch fishes, especially sharks, have used mass-balance ecosystem models (e.g., Ecopath with Ecosim (Walters et al., 1997)), based on assessment of direct density-dependent effects, and have produced contrasting results. Manickchand-Heileman et al. (1988) concluded that although sharks occupy the highest trophic levels in the Gulf of Mexico, the effect of an increase in their population size on the rest of the community is small. Kitchell et al. (2002) found that oceanic sharks are not key species in the north central Pacific Ocean, and Carlson (2007) also found that a population reduction of sharks in Apalachicola Bay in the Gulf of Mexico did not result in strong top-down effects such as trophic cascades. In contrast, Stevens et al. (2000), García-Gómez (2000), and Fernández et al. (2001) found that changes in abundance of different shark species resulted in changes of different magnitude and wide spectrum in their respective communities.

Stevens et al. (2000) proposed that the strongest responses to shark removals do not always take place in populations of their main prey, and thus their regulatory role is not necessarily related to the relative contribution of a prey to their diet (i.e., direct effects). These authors recognized the need to characterize the trophic interactions of these species and assess their importance as spreading mechanisms of indirect effects and thus in regulating marine communities. Myers et al. (2007) identified batoids as major contributors to indirect trophic effects (i.e., a trophic cascade) in an Atlantic marine ecosystem that became considerably unbalanced as a result of exploitation of top predators, proposing an important role of batoids as mesopredators.

Most of these analyses focused on functional approaches, i.e., quantification of the functional importance of species in a community (Libralato et al., 2006), to study the effect of a predator on the population size of its prey, or, in some very specific cases, on trophic cascade effects that do not consider other types of indirect effects (e.g., apparent competition, competitive exclusion), which have also been identified as strong forces shaping community structure (Menge, 1995). A different option for analyzing trophic networks is the structural perspective, i.e., quantification of the positional importance of trophic groups in a trophic flow network (Wassermann and Faust, 1994, Jordán, 2003, Jordán et al., 2006), which allows identification of those species that play an important role in structuring the ecosystem, referred to as key species (Dunne et al., 2002a, Jordán and Scheuring, 2002). The purpose of the present study was to assess the importance of elasmobranch species in the marine ecosystem of the central coast of the Colombian Pacific Ocean using the structural approach of topological analysis of trophic networks.