African mammals, foodwebs, and coexistence.

In the 65 million years since a mass extinction led to the demise of dinosaurs, evolution has generated amazingly diverse and complex foodwebs on each continent (1). These foodwebs contain hundreds to thousands of interacting species, each linked to other species either by feeding on them or by being fed on by them. However, it has been difficult to determine consumer diets across seasons, individuals, and space, and especially hard to quantify the strengths of these linkages in all but the simplest foodwebs. These issues have limited the ability of ecologists to understand how foodwebs are structured, how so many interacting species can coexist, and how the patterning and strengths of these linkages determine the stability of foodwebs (2). The use of next-generation sequencing is emerging as a key tool for quantifying, with fine resolution, the diet composition of consumers (3). By using these high-throughput techniques on fecal samples from large African herbivore species to quantify their diets, Kartzinel et al. (4) provide important insights into foodweb structure and coexistence in one of the few remaining terrestrial foodwebs that still has its full complement of large mammals. In particular, Kartzinel et al. (4) extracted DNA from the feces of seven large African herbivores—the African elephant, impala, two species of zebra, buffalo, Boran cattle, and dik-dik—within a 150 km portion of Kenyan savanna (Fig. 1). To determine diets of each species, they obtained from 27 to 52 fecal samples per species during a single season. DNA metabarcoding allowed them to quantify the relative dietary abundances of about 100 different plant species or genera, thus demonstrating the efficacy of this approach for coexisting mammals. They found surprisingly strong dietary differences among these herbivore species. This dietary niche differentiation can explain the stable coexistence of these competing species. An earlier study that used carbon isotopes in feces was able to quantify abundances of two major groups of plants, grasses, and browse, and showed that many (but not all) herbivore species were separated along a gradient defined by the ratio of these two plant groups (5). Kartzinel et al. (4) have provided the finest-resolution evidence to date demonstrating that each large African herbivore species consumes a suite of plant species different from the suite consumed by other cooccurring herbivore species. Why is this so important? The work of Kartzinel et al. (4) suggests that the performance of a given herbivore species depends not on how much “forage” a grassland or savanna may contain but on the actual abundances of those particular plant species on which that herbivore specializes. For example, the plains zebra and Grevy’s zebra both mainly eat grass and thus would seem to be strong competitors. However, Kartzinel et al. found that there were 14 grass species and a forb species upon which these two competitors were niche differentiated, with 10 of these plant species mainly eaten by Grevy’s zebra and 5 mainly eaten by the plains zebra. Why does this dietary differentiation lead to coexistence? Clearly, by eating different plant species, each herbivore species reduces the abundances of its own preferred food plant species more than it reduces the abundances of the preferred food for the other species. This dietary differentiation meets the classic ecological criterion for the coexistence of competing species: that each species inhibits itself more than it inhibits the other species. However, because of the multiple linkages and potential feedback paths in foodwebs, cause and effect relations are rarely so simple (6–9). These 15 plant species likely compete with each other. When Grevy’s zebras are at high abundance, they will cause their 10 favored plant species to be rarer. The five plant species preferentially consumed by the plains zebra might then increase in abundance because of reduced competition, which would benefit the plains zebra. A similar process could cause high densities of plains zebras to benefit Grevy’s zebras. These indirect effects, mediated by competitive interactions among plants for their own limiting resources (water, nitrogen, phosphorus, light, etc.), would enhance the ability of two seemingly close competitors to stably coexist. Indeed, the net effect of each of the zebra species on the other might actually become positive and form an “indirect mutualism” if the competitive interactions among the 15 plant species were strong (7). Achieving a more mechanistic and predictive understanding of foodwebs is one of the major challenges facing ecology. A foodweb is a complex network influenced by the intensity of species interactions, which themselves quantitatively depend on the tradeoffs each species faces in dealing with top-down forces (e.g., from its predators or disease), bottom-up forces (from competition Fig. 1. African mammals studied range in size from elephants (Top), to Grevy’s zebra (Middle), to the dik-dik (Bottom). Images courtesy of Andrew Dobson (Department of Ecology and Evolutionary Biology, Princeton University).