Ecological pork: novel resources and the trophic reorganization of an ecosystem.

P of the attraction of ecology and its related intellectual challenges is its dynamic complexity. Darwin’s (1) entangled bank metaphor captured the essence; it wasn’t just that everything was connected to everything else but rather that specific relationships mattered. Darwin found that mowed turf contained approximately twice as many species as unmowed turf; a logical chain of influence was argued to link the probability of clover pollination and seed production to the negative influence of domestic cats on mice, themselves major predators of bumble bees doing the pollinating. Since Darwin’s time an ever-increasing array of field experiments and observations has substantiated the dynamic consequences of these connections, especially in aquatic systems (2–6). These and many comparable examples share the common feature of highlighting the importance of apex predators and therefore top-down trophic control of population dynamics and community structure. In many cases, chains of indirect interactions among species with shared predators intensify top-down control. Effects are particularly acute when these relationships are asymmetric; one species may be a significant energy source for a predator without being regulated by it, thus strengthening the predatory impacts on other prey (7). Change is commonplace in ecosystems with awareness heightened by the consequences of introductions of exotic or nonnative species or range expansions of those native to the system. The research contribution by Roemer et al. in this issue of PNAS (8) adds a novel dimension to the complexity of responses to biological invasions. The presence of feral, nonnative pigs seems to have enabled golden eagles to colonize some of California’s Channel Islands, resulting in restructuring of an island food web and the approaching extinction of an endangered native fox. A hypothesis is proposed that native spotted skunks compete with foxes; piglets bolster eagle predation on foxes, thus releasing skunks from competitive suppression, leading to their recent numerical increase. The study is exceptional for its demonstration that birds, taxa that are often discounted within terrestrial ecosystems as important apex predators (9) that benefit from highly productive alternative prey (piglets), can increase to the point that their predation on native foxes becomes a significant conservation concern. Darwin’s interest in chains of interactions and the related indirect positive or negative consequences once again is justified. The Roemer et al. study is unusual on a number of grounds. Long-term interest in the biology of the Channel Islands provides an important historical perspective. The islands themselves could be perceived as replicates, although this attribute was minimally developed. The authors also support their conclusions with an intriguing and broad sampler of ecology’s tools: natural history, including sniffing livetrapped golden eagles for the telltale odors of skunk encounters; a three trophic-level modeling effort based on Lotka-Volterra dynamics, which supports some but not all the population trajectories; intense long-term live-trapping and mark-recapture efforts that revealed the reciprocal trends in fox and skunk densities; diet studies of what this intriguing mix of carnivores eat; bioenergetics estimates of predation rates by interacting species; and stable isotope analyses (N and C) to suggest energy sources independent of the carcass count on which the eagle diet is based. The temporal and spatial breadth (1993–1999, with two separate sites on Santa Cruz), and the essential commitment underlying this study are impressive—hundreds of hours trapping, marking, and releasing foxes and skunks and the endless details of determining diets and finding corpses. Similar to any detailed, condensed report, some questions remain unanswered, and others are roused. For instance, the stable isotope analyses suggest that the eagle diet consists of more than just piglets, foxes, and an occasional skunk. It seems likely that sea birds such as cormorants and pelicans, available and probably increasing since 1968 (10) following recovery from the DDT-induced eggshell thinning, provide alternative prey. The assumption that foxes and spotted skunks compete based solely on calculated dietary overlap and consumption rates is unconvincing, because it does not address whether the overlapping resources are in short supply and therefore competed for. In fact, is this premise even necessary to their argument? Their simulation model, although correctly portraying the inverse population trajectories of eagles and foxes, fails for skunks. Feral pigs have inhabited these islands for over 150 years. What delayed the colonization of golden eagles until 1994? In the early 1900s, the Channel Islands were home to vigorous populations of bald eagles. In fact, they became the quarry of island sheep farmers who were losing their lambs to marauding eagles (11). Were lambs bolstering bald eagles in ways similar to the piglet-golden eagle example? Observed agonistic encounters between these eagle species suggest no pattern of dominance (12). The long-delayed golden eagle invasion suggests unrecognized dimensions to their interesting story. For instance, island foxes seem especially vulnerable to ectoparasite infections (13) and even diseases spread by agricultural animals (11). And what hidden role do the pigs play? This species is widely documented to be environmentally destructive at most sites to which they’ve been introduced (14, 15). Many unanswered questions are stimulated by the case study described by Roemer et al.