Variable infection of stream salamanders in the southern Appalachians by the trematode Metagonimoides oregonensis (family: Heterophyidae).

Many factors contribute to parasites varying in host specificity and distribution among potential hosts. Metagonimoides oregonensis is a digenetic trematode that uses stream-dwelling plethodontid salamanders as second intermediate hosts in the Eastern US. We completed a field survey to identify which stream salamander species, at a regional level, are most likely to be important for transmission to raccoon definitive hosts. We surveyed six plethodontid species (N = 289 salamanders) from 23 Appalachian headwater sites in North Carolina: Desmognathus quadramaculatus (n = 69), Eurycea wilderae (n = 160), Desmognathus ocoee (n = 31), Desmognathus monticola (n = 3), Eurycea guttolineata (n = 7), and Gyrinophilus porphyriticus (n = 19). We found infection in all species except D. monticola. Further analysis focused on comparing infection in the two most abundant species, D. quadramaculatus and E. wilderae. We found that D. quadramaculatus had significantly higher infection prevalence and intensity, probably due to a longer aquatic larval period and larger body sizes and thus greater cumulative exposure to the parasite.

Spatial scale and structure of complex life cycle trematode parasite communities in streams.

By considering the role of site-level factors and dispersal, metacommunity concepts have advanced our understanding of the processes that structure ecological communities. In dendritic systems, like streams and rivers, these processes may be impacted by network connectivity and unidirectional current. Streams and rivers are central to the dispersal of many pathogens, including parasites with complex, multi-host life cycles. Patterns in parasite distribution and diversity are often driven by host dispersal. We conducted two studies at different spatial scales (within and across stream networks) to investigate the importance of local and regional processes that structure trematode (parasitic flatworms) communities in streams. First, we examined trematode communities in first-intermediate host snails (Elimia proxima) in a survey of Appalachian headwater streams within the Upper New River Basin to assess regional turnover in community structure. We analyzed trematode communities based on both morphotype (visual identification) and haplotype (molecular identification), as cryptic diversity in larval trematodes could mask important community-level variation. Second, we examined communities at multiple sites (headwaters and main stem) within a stream network to assess potential roles of network position and downstream drift. Across stream networks, we found a broad scale spatial pattern in morphotype- and haplotype-defined communities due to regional turnover in the dominant parasite type. This pattern was correlated with elevation, but not with any other environmental factors. Additionally, we found evidence of multiple species within morphotypes, and greater genetic diversity in parasites with hosts limited to in-stream dispersal. Within network parasite prevalence, for at least some parasite taxa, was related to several site-level factors (elevation, snail density and stream depth), and total prevalence decreased from headwaters to main stem. Variation in the distribution and diversity of parasites at the regional scale may reflect differences in the abilities of hosts to disperse across the landscape. Within a stream network, species-environment relationships may counter the effects of downstream dispersal on community structure.

Seasonal and Annual Variation in Trematode Infection of Stream Snail Elimia proxima in the Southern Appalachian Mountains of Virginia.

Understanding temporal variation of host-pathogen dynamics can be important for predicting disease risks and anticipating how disease systems may change in response to natural or human disturbances. Seasonal changes in weather, especially those associated with changes in temperature or precipitation, are often a key component of temporal changes in infection risk and can have important impacts on disease systems. However, these patterns can be difficult to track due to interannual variation and the need for longer term, multi-year surveillance efforts. We assessed seasonal and annual changes in the trematode component community of first-intermediate host stream snail Elimia (= Oxytrema = Goniobasis) proxima across 5 streams in the southern Appalachian Mountains. Over 3 yr, we found no evidence of consistent seasonal peaks of trematode infection in E. proxima. There was some across-site consistency in infection prevalence over 4 yr, because high prevalence sites tended to maintain higher prevalence from year to year, relative to lower prevalence sites. In addition, we examined the relationship between prevalence of first-intermediate host infection, weather variables, and site-level factors, including snail density and water quality metrics. Trematode prevalence was negatively related to total precipitation, which may have been due to the movement of infectious parasite stages and hosts downstream during high flows. We found no strong relationships between trematode prevalence and snail density or any of the water quality metrics examined in this study, indicating that snail infection may be driven primarily by definitive host activity.

Host density and competency determine the effects of host diversity on trematode parasite infection.

Variation in host species composition can dramatically alter parasite transmission in natural communities. Whether diverse host communities dilute or amplify parasite transmission is thought to depend critically on species traits, particularly on how hosts affect each other's densities, and their relative competency as hosts. Here we studied a community of potential hosts and/or decoys (i.e. non-competent hosts) for two trematode parasite species, Echinostoma trivolvis and Ribeiroia ondatrae, which commonly infect wildlife across North America. We manipulated the density of a focal host (green frog tadpoles, Rana clamitans), in concert with manipulating the diversity of alternative species, to simulate communities where alternative species either (1) replace the focal host species so that the total number of individuals remains constant (substitution) or (2) add to total host density (addition). For E. trivolvis, we found that total parasite transmission remained roughly equal (or perhaps decreased slightly) when alternative species replaced focal host individuals, but parasite transmission was higher when alternative species were added to a community without replacing focal host individuals. Given the alternative species were roughly equal in competency, these results are consistent with current theory. Remarkably, both total tadpole and per-capita tadpole infection intensity by E. trivolvis increased with increasing intraspecific host density. For R. ondatrae, alternative species did not function as effective decoys or hosts for parasite infective stages, and the diversity and density treatments did not produce clear changes in parasite transmission, although high tank to tank variation in R. ondatrae infection could have obscured patterns.

Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts.

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free-living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host-parasite-predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.