Fishing drives declines in fish parasite diversity and has variable effects on parasite abundance

Abstract

Despite the ubiquity and ecological importance of parasites, relatively few studies have assessed their response to anthropogenic environmental change. Heuristic models have predicted both increases and decreases in parasite abundance in response to human disturbance, with empirical support for both. However, most studies focus on one or a few selected parasite species. Here, we assess the abundance of parasites of seven species of coral reef fishes collected from three fished and three unfished islands of the Line Islands archipelago in the central equatorial Pacific. Because we chose fish hosts that spanned different trophic levels, taxonomic groups, and body sizes, we were able to compare parasite responses across a broad cross section of the total parasite community in the presence and absence of fishing, a major human impact on marine ecosystems. We found that overall parasite species richness was substantially depressed on fished islands, but that the response of parasite abundance varied among parasite taxa: directly transmitted parasites were significantly more abundant on fished than on unfished islands, while the reverse was true for trophically transmitted parasites. This probably arises because trophically transmitted parasites require multiple host species, some of which are the top predators most sensitive to fishing impacts. The increase in directly transmitted parasites appeared to be due to fishing-driven compensatory increases in the abundance of their hosts. Together, these results provide support for the predictions of both heuristic models, and indicate that the direction of fishing's impact on parasite abundance is mediated by parasite traits, notably parasite transmission strategies.

Human impacts decouple a fundamental ecological relationship—The positive association between host diversity and parasite diversity

“…Previous studies have shown strong divergence in the fish communities between these three fished and three unfished islands, with higher fish biomass and abundance of top predators on unfished islands, and higher abundance of low trophic‐level fishes like planktivores on fished islands, possibly due to release from predation pressure (DeMartini, Friedlander, Sandin, & Sala, ; Sandin et al., ). Island size, latitude, average sea surface temperature, and productivity are not correlated with fishing pressure among the six islands, and pooling data within the three fished and three unfished islands allows us to homogenize the influence of oceanographic factors across the archipelago (Sandin et al., ; Wood, Sandin, et al., ; Wood et al., ). This system is therefore a suitable natural experiment for testing the impacts of fishing‐driven environmental change on a variety of ecosystem parameters, including host and parasite biodiversity.…”

“…All sampling was conducted at between two and 10 sites within each island, as conditions permitted [see appendix C in Wood, Sandin, et al. ()]. By logistical necessity, host biodiversity surveys and host collections were conducted separately.…”

“…At each of these six islands, we sampled seven species of reef fishes ( Cephalopholis urodeta , Acanthurus nigricans , Ctenochaetus marginatus , Paracirrhites arcatus , Stegastes aureus , Chromis margaritifer , and Pseudanthias bartlettorum ). The seven host species span a variety of body sizes, represent important trophic and taxonomic groupings, and include only broadly distributed species present at most reefs in the region (Wood, Sandin, et al., ; Wood et al., ). To maximize our scope of inference, we selected focal host species that represent a cross‐section of coral reef fish biodiversity, allowing us to obtain an optimally representative subset of parasite species.…”

“…Because habitat type and wave exposure of collection sites might influence estimates of parasite abundance, we attempted to hold these variables constant by conducting most sampling on the leeward forereef of each island at depths between 11 and 18 m [see appendices C and D in Wood, Sandin, et al. ()]. We recorded several items of meta‐data for each fish, including total length, standard length, fork length, and mass.…”

Environmental change and the ecology of infectious disease

“…As a Ph.D. student, I used exploited marine fishes and their metazoan parasites as a model system to explore this question, first generating several hypotheses ( 1), and then testing these hypotheses by using fished and unfished coral islands of the Line Islands archipelago as replicates in a natural experiment. This work showed that fishing can increase the abundance of some parasite taxa and decrease the abundance of others, depending on parasite traits ( 2,3). Specifically, parasites with complex life cycles were vulnerable to fishing-driven declines, probably because they require multiple host species, some of which are the top predators most sensitive to fishing impacts.…”