Ecology, 95(7), 2014, pp. 1929–1946 Ó 2014 by the Ecological Society of America Fishing drives declines in fish parasite diversity and has variable effects on parasite abundance 1,3 2 2 1 1 CHELSEA L. WOOD, STUART A. SANDIN, BRIAN ZGLICZYNSKI, ANA SOFI´A GUERRA, AND FIORENZA MICHELI 1Department of Biology, Stanford University, Stanford, California 94305 USA 2Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California 92037 USA 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. Key words: anthropogenic environmental change; biodiversity; disease; disturbance; fishing; parasites. INTRODUCTION Preston et al. 2013), and redirect energy flow within and For the past several decades, ecologists have worked among food webs by behaviorally manipulating (e.g., to document impacts of anthropogenic environmental Lafferty and Morris 1996, Sato et al. 2011) or killing change on the distributions of free-living species. But (Suttle 2005) their hosts. Given their influence, change in despite the ubiquity of parasites,which constitute at least parasite abundance is likely to have reverberating 40% of animal species on the planet (Dobson et al. 2008) impacts on ecosystem function (Gomez et al. 2012). and make up the majority of species in 27 of its 42 Second, understanding the impacts of anthropogenic environmental change on the abundance and diversity of recognized animal phyla (Poulin and Morand 2000, parasites gives us insight into current and future disease deMeeus and Renaud 2002), we still have only a risk for hosts of special concern, like humans (Keesing et rudimentary understanding of how human impacts al. 2010), commercially valuable domestic (Cleaveland et affect parasite abundance and diversity. Understanding al. 2001), and wild (McCallum et al. 2005, Shields 2012) how parasite biodiversity will change in a changing animals, and endangered species (Daszak 2000). For a environment is important for a number of reasons. First, full accounting of the impacts of human activities on a growing body of evidence suggests that parasites are ecosystems and for projecting future disease risk, it is ecologically influential in some ecosystems (Gomez et al. therefore critical that ecologists answer the question: 2012). They can regulate host populations (e.g., Hudson How does anthropogenic environmental change impact et al. 1998), mediate the species composition of free- parasite abundance and diversity? living communities (e.g., Mouritsen and Poulin 2005, Only a few empirical studies have assessed the effects Wood et al. 2007), comprise a substantial proportion of of human disturbance across a broad range of parasite the total biomass of an ecosystem (e.g., Kuris et al. 2008, species, and these tend to find mixed responses to disturbance. In the Atlantic lowlands of Costa Rica, Manuscript received 2 July 2013; revised 6 November 2013; McKenzie (2007) found that, among three species of accepted 10 December 2013; final version received 6 January amphibian hosts collected from clear-cut cattle pasture 2014. Corresponding Editor: M. H. Carr. 3 Present address: Department of Ecology and Evolution- and forest habitats, six metazoan parasite species were ary Biology, University of Colorado, Boulder, Colorado more abundant in pasture than forest, two species were 80309 USA. E-mail: [email protected] more abundant in forest than pasture, and 13 species did 1929 1930 CHELSEA L. WOOD ET AL. Ecology, Vol. 95, No. 7 not differ significantly between the two habitats. Aeby et population, reducing transmission of its directly trans- al. (2011) found that, while prevalence of growth mitted parasite and resulting in lower parasite abun- anomalies (a tumor-like disease of unknown etiology) dance on fished than on unfished islands. Indirect effects of Porites spp. corals increased with increasing density of fishing include fishing the predator or competitor of a of nearby human populations across the Hawaiian host, which can cause compensatory increases in host Islands, the prevalence of trematodiasis (infection by density (e.g., DeMartini et al. 2008), increasing trans- trematode metacercariae) decreased across this impact mission of a directly transmitted parasite, and resulting gradient. A number of studies have compared parasite in higher abundance on fished than on unfished islands. prevalence and diversity between marine reserves, where We use the word ‘‘fishing’’ to refer to the ecosystem-level human environmental impacts are legally excluded, and effects of fishing, not just its host-population-level open-access areas where such impacts continue. Some effects, and the term therefore encompasses both the have found higher parasite abundance and diversity in direct and indirect effects of fishing on hosts and non- reserves than in open-access areas (Sasal et al. 1996, hosts. Bartoli et al. 2005, Loot et al. 2005, Hechinger et al. A previous study conducted in the Line Islands system 2008, Wood et al. 2013), while others have found higher examined the parasite communities of five reef fishes parasite abundance in open-access areas (Sonnenholzner from one fished (Kiritimati) and one unfished (Palmyra) et al. 2011), or have failed to find significant differences island, finding higher parasite richness in all host species in abundance and diversity between reserve and open- at the unfished island (Lafferty et al. 2008). Lafferty et access areas (Ternengo et al. 2009). In a meta-analysis, al. (2008) also found higher abundance on the fished Lafferty (1997) showed that the overall response of than the unfished island for two parasite taxa, higher aquatic parasites to pollution impacts is weak, primarily abundance on the unfished than the fished island for because parasite groups diverge in their responses to seven other taxa, and no significant differences for the 16 pollution, and different types of pollution impacts (e.g., remaining taxa detected. While these effects could be eutrophication vs. heavy metal contamination) can driven by fishing, they could also be due to other generate divergent responses of abundance within differences between the islands, including oceanography parasite groups. Together, these results suggest that or biogeography. We thus designed a natural experiment the response of parasites to environmental change is by replicating within each level of the fishing ‘‘treat- variable and context specific. But several key questions ment,’’ that is, by expanding the experimental design remain. First, when we look across a wide diversity of from one fished and one unfished island to three fished parasite taxa, will most populations increase, decrease, and three unfished islands, with the goal to decouple or remain unchanged in response to anthropogenic fishing effects from the physical and oceanographic impacts? Second, what taxonomic groups of parasites differences among the sampled islands. This allowed us tend to exhibit sensitivity to anthropogenic impacts, to attribute observed differences between levels of the what groups tend to increase in abundance as impacts fishing ‘‘treatment’’ to the effect of fishing and to rule accumulate, and what characteristics might drive these divergent responses? out other sources of inter-island variability. For each of To address these questions, we focused on a marine our research questions, we formulated several a priori model system affected by fishing (Sandin et al. 2008), hypotheses originating from previous findings (Lafferty one of the most intense and longest-standing impacts on et al. 2008), as well as from theoretical (Keesing et al. the world’s oceans (Jackson et al. 2001, Halpern et al. 2006, Dunn et al. 2009, Colwell et al. 2012, Lafferty 2008). We aimed to test how fishing-driven alterations in 2012) and synthetic (Wood et al. 2010) work. the fish community affect the abundance, species Question 1: How does richness of parasite taxa differ