Comparative studies of host-parasite relationships have shown tremendous potential for illuminating the underlying mechanisms of speciation, dispersal, gene flow, effective population size, and both evolutionary and ecological patterns of occurrence that might otherwise remain obscure (Biek et al. 2006, Blakeslee et al. 2008, McCoy et al. 2005, Nieberding et al. 2005, Whiteman and Parker 2005, Whiteman et al. 2007, Wirth et al. 2005). Their emerging use in untangling ecosystem dynamics and answering questions pertaining to host ecology, coupled with recent increases in research on cave systems and their fauna draw cause for concern to the paucity of empirical investigations. Literature reviews have revealed limited data regarding parasites of cave fish species, with reports primarily confined to bat ectoparasites (Kurta et al. 2007, Poissant and Broders 2008), and incidences reported in select specimens or species of cavefishes, salamanders, and beetles (Fenolio et al. 2013, Hendrickson et al. 2001, McAllister et al. 2006, Santamaria and Faille 2007, Niemiller and Poulson 2010, McAllister et al. 2013). The largely unreported role of parasites in cave ecosystems limits the application of practical aquatic ecology conceptions and the validity of connectivity studies that do not account for parasitism and energy transfer in these harsh and highly specialized environments.

In cave systems, food scarcity is often cited as a key ecological factor with respect to persistence and resilience for many populations (Eigenmann 1909, Poulson 1963, Poulson and Lavoie 2000, Trajano 2001, Culver and Pipan 2009). It is estimated that only 0.001% of the energy available to surface systems is available to subterranean habitats (Aley and Aley 1979). Such a restricted direct energy supply forces many cave taxa to rely more heavily on energetic input from the surface through indirect means such as plant debris, detritus, dissolved organics (Ginet and Decou 1977, Langecker 2000, Venarsky et al. 2012), and cannibalism. Many animals living in subterranean habitats are opportunistic feeders that consume a wide variety of prey items and with inconsistent regularity due to stochastic conditions underground (Trajano 2001).

With such variable ecosystem dynamics, the success of parasites of cave fauna is largely dependent on ecology of both the host and parasite. Definitive host specialization, paratenic host requirements, and host biogeography can all affect parasite survival (Seneviratne et al. 2009). Host allopatry, or isolation, may limit transmissibility of parasites between hosts, therefore restricting dispersal potential and successful colonization of primary host populations (Dick and Patterson 2007). In conjunction with the already limited diversity of cave taxa available for parasite utilization, opportunities to colonize additional or alternative hosts are much narrower than in more specious systems. Similarly, potential paratenic host species for parasites with oligoxenous life cycles may also be reduced, further limiting the diversity and likelihood of successful colonization of cave taxa.

Grotto Sculpin (Cottus specus) have recently been distinguished from the Banded Sculpin species complex (Cottus carolinae) and areendemic to cave systems underlying Perry County, Missouri (Adams et al. 2013, Day et al. in press). These uniquely cave-adapted fish are state-threatened and listed as endangered in the United States under the Endangered Species Act (USFWS 2013). Preliminary investigations of Grotto Sculpin parasite diversity uncovered an elevated occurrence of acanthocephalans in cave-dwelling fish populations as compared to surface-dwelling Banded Sculpin (Day and Gerken, unpublished data). Acanthocephalan worms are primarily intestinal parasites that employ a spiny proboscis for attachment to their fish, bird, or mammalian hosts (Kennedy 2006). When found in high concentrations, as they often are in other cottids (Muzzall and Bowen 2002), acanthocephalans have been shown to negatively affect the condition of their host (Kennedy 2006). Infection rates by these worms vary in conjunction with water quality parameters, and may therefore serve as biomarkers or indicators of the degree of environmental stress fish are facing and can be used as an index of overall fish health (Galli et al. 2001, Kahn 2004).

In this study, we provide one of the first dedicated investigations of cavefish parasite ecology and explore the efficacy of parasites for comparing habitat-specific infection rates as indicators of the prevalence of fish parasites in cave ecosystems. In Grotto Sculpin, we sought to identify potential at-risk populations and those most susceptible to environmental perturbations from surface ecosystems by comparing relative parasite loads between cave and surface populations of Cottus specus. We hypothesized that decreased parasite loads would be present in cave populations due to limited food web exploitation and resulting difficulties in locating appropriate paratenic hosts.

Our observation of what appears to be a successful invasion of the cave environment by acanthocephalans marks the first report of parasitism in a cave-dwelling sculpin and the most inclusive of all cavefish species. Our results revealed that parasitism by Leptorhynchoides thecatus was significantly higher in caves than non-cave stream populations of Grotto Sculpin. While small sample sizes precluded fine-scale resolution of host-parasite population dynamics in individual caves, our data were sufficient to provide an overview of possible explanations for this unique phenomenon that encompass multiple schools of ecological and evolutionary thought. Here we briefly explore the biological relationships of cannibalism and parasitism, complemented by an account of how their ecological effects may be compounded and magnified by the perils of subterranean life within the context of conservation.

Subterranean systems have traditionally been thought of as simple, unchanging ecosystems that persist in near or total isolation from surface resources, but this assumption has been the subject of much scrutiny and reconsideration in recent years as studies of nutrient contributions and trophic ecology increase (Huntsman et al. 2011, Schneider et al. 2011, Venarsky et al. 2012). Taxonomic diversity in these harsh environments continues to be revealed (Niemiller and Zigler 2013), as do concerns for their timely descriptions and the implementation of conservation measures (Niemiller et al. 2013).

The cave system inhabited by Grotto Sculpin, is remarkably interconnected and influenced by surface activities and supports the notion of increased complexity. Just as organic matter beneficial to troglobites may enter caves relatively quickly in shallow karst regions, so too can potential contaminants from surface land use practices. Fox et al. (2010) found that Perry County caves were subject to increased levels of urban and agricultural runoff, and sinkholes remain one of the greatest potential threats to Grotto Sculpin. Pesticides, herbicides, metals, and organic waste known to be detrimental to vertebrate physiology that leak into subterranean streams via sinkholes are all likely to have negative impacts on Grotto Sculpin populations, including increasing susceptibility to parasite infection due to reduced condition or health (Khan 2004, Marchand et al. 2012, Kleinertz and Palm 2013). Strengthening these concerns for Grotto Sculpin in particular are new recharge delineation data and vulnerability analyses that suggest overflow between cave systems occurs with some degree of regularity and severity in these systems (Moss 2013).

Point- and nonpoint-source pollution events pose notable threats to Grotto Sculpin populations and could increase susceptibility to parasitism as a result of reduced health condition. Mystery Cave supports the largest documented population of Grotto Sculpin, with estimates ranging from 262 to 509 individuals (Day et al. 2009). This cave has experienced at least one recent mass extirpation event from a point-source pollution event in 2005 when a cow carcass was washed into the cave stream and dissolved oxygen levels dropped below critical levels for fish survival. Burr et al. (2001) also reported a mass extirpation event in Running Bull Cave, the origin of which remains unknown but is suspected to be anthropogenic in nature. Although population abundances in both of these caves appear to be high at present, these data do provide support for continued investigation of fish health and condition in relation to water quality and available food resources.

In these unique karst systems, extensive movement of groundwater serves not only as a means of nutrient transport and fish translocation, but also as means of increasing parasite dispersal and both nutrient and pollution transport. Mertz Cave, which had the lowest incidence of parasitism for a cave, has the largest and most accessible inflowing entrance relative to the other caves tested, which may allow for a higher influx of nutrients from the surface. This may result in less cannibalism and therefore less parasitism (Table 1). In remote or isolated regions of this cave system, a lower influx of surface energy could offer a narrow range of possible hosts for parasites. Therefore, Leptorhynchoides thecatus could be more likely to parasitize Grotto Sculpin in stream reaches located in far proximity to allochthonous organic input. Coupled with cannibalism, this may also contribute to the elevated rates of parasitism we observed.

Cannibalism is theorized to promote parasitism (Hatcher et al. 2008), and when considered in conjunction with environmental variability may increase as a function of food scarcity. Amphipods are widely recognized as a common paratenic or intermediate host for acanthocephalans, and represent the primary prey item available to Grotto Sculpin (Gerken, unpublished data). Seasonal or condition-dependent abundance and diversity of available prey items in this system could lead to diet constriction and increased the reliance of Grotto Sculpin on cannibalism, and thus likelihood of parasite infection. Further investigation of trophic dynamics and food web structure in Perry County caves is necessary to test this hypothesis.

In addition to providing insight on the ecology of Grotto Sculpin and their acanthocephalan parasites, the results of this work elucidate novel data gaps on parasite ecology and their persistence in cave fauna. The results of this study suggest that researchers and managers should take care to investigate the potential influences of parasitism and variation in surface contributions to cave biodiversity population dynamics. Directed studies of the prevalence and epidemiological implications of fish health and parasite infections in cave species are still limited in scope and in need of further inquiry. Future research should seek to understand the population dynamics of parasites in subterranean systems and their impacts on ecosystem ecology and function.