Founder effects and species introductions: A host versus parasite perspective.

Species colonizations (both natural and anthropogenic) can be associated with genetic founder effects, where founding populations demonstrate significant genetic bottlenecks compared to native populations. Yet, many successfully established free-living species exhibit little reduction in genetic diversity-possibly due to multiple founding events and/or high propagule pressure during introductions. Less clear, however, is whether parasites may show differential signatures to their free-living  hosts. Parasites with indirect life cycles may particularly be more prone to founder effects (i.e., more genetically depauperate) because of inherently smaller founding populations and complex life cycles. We investigated this question in native (east coast) and introduced (west coast) North American populations of a host snail Tritia obsoleta (formerly Ilyanassa obsoleta, the eastern mudsnail) and four trematode parasite species that obligately infect it. We examined genetic diversity, gene flow, and population structure using two molecular markers (mitochondrial and nuclear) for the host and the parasites. In the host snail, we found little to no evidence of genetic founder effects, while the trematode parasites showed significantly lower genetic diversity in the introduced versus native ranges. Moreover, the parasite's final host influenced infection prevalence and genetic diversity: Trematode species that utilized fish as final hosts demonstrated lower parasite diversity and heightened founder effects in the introduced range than those trematodes using birds as final hosts. In addition, inter-regional gene flow was strongest for comparisons that included the putative historical source region (mid-Atlantic populations of the US east coast). Overall, our results broaden understanding of the role that colonization events (including recent anthropogenic introductions) have on genetic diversity in non-native organisms by also evaluating less studied groups like parasites.

Large-scale spatial variation in parasite communities influenced by anthropogenic factors.

Parasites are integral members of natural communities, but large-scale determinants of their abundance and diversity, including the importance of biotic and abiotic factors, both natural and anthropogenic, are often not well understood. Here, we examine which factors best predict larval trematode communities in the mudsnail host Ilyanassa obsoleta across a regional landscape. At 15 salt marsh sites spanning 200 km, we quantified the diversity of trematodes and the prevalence (i.e., proportion) of infected hosts and sampled a broad array of potential parasite predictors including abundance of intermediate and definitive hosts, habitat, nutrients, metals, roads, and sediment characteristics. We identified the set of best performing models to explain variability associated with five metrics of trematode prevalence and diversity using an information-theoretic approach. Results indicate that several anthropogenic factors associate with this trematode community and that the direction of their influence differs. Road density around sites was a strong negative predictor of all trematode prevalence and species richness metrics. Nitrogen, another human influenced variable, was a strong positive predictor for the most abundant trematode species in the system. In addition, the abundance of definitive fish hosts was a positive predictor in several models, confirming the importance of this direct biological link to parasites. Other influential variables included sediment composition and heavy metals (arsenic, copper, lead, and zinc). We discuss possible direct and indirect mechanisms to explain these findings including that anthropogenic factors may be directly influencing free-living stages of trematodes, or be acting as proxies of hard-to-measure hosts.

The Marine Mammal Protection Act at 40: status, recovery, and future of U.S. marine mammals.

Passed in 1972, the Marine Mammal Protection Act has two fundamental objectives: to maintain U.S. marine mammal stocks at their optimum sustainable populations and to uphold their ecological role in the ocean. The current status of many marine mammal populations is considerably better than in 1972. Take reduction plans have been largely successful in reducing direct fisheries bycatch, although they have not been prepared for all at-risk stocks, and fisheries continue to place marine mammals as risk. Information on population trends is unknown for most (71%) stocks; more stocks with known trends are improving than declining: 19% increasing, 5% stable, and 5% decreasing. Challenges remain, however, and the act has generally been ineffective in treating indirect impacts, such as noise, disease, and prey depletion. Existing conservation measures have not protected large whales from fisheries interactions or ship strikes in the northwestern Atlantic. Despite these limitations, marine mammals within the U.S. Exclusive Economic Zone appear to be faring better than those outside, with fewer species in at-risk categories and more of least concern.

Using parasitic trematode larvae to quantify an elusive vertebrate host.

Digenean trematode parasites require multiple host species to complete their life cycles, and their abundance can often be strongly correlated with the abundance of their host species. Species richness and abundance of parasites in easily sampled host species may yield an accurate estimate of the species richness and abundance of other hosts in a parasite's life cycle that are difficult to survey directly. Accordingly, we investigated whether prevalence and mean abundance of trematodes could be used to estimate the abundance of one of their host species, diamondback terrapins (Malaclemys terrapin), which are difficult to sample and are designated as near threatened (by the International Union for Conservation of Nature [IUCN Red List]) along some U.S. coasts. As an adult the trematode Pleurogonius malaclemys is specific to terrapins. Its larval stages live first inside mud snails (Ilyanassa obsoleta) and are subsequently shed into the environment where they form external metacercarial cysts on hard surfaces such as snail opercula. The life cycle of P. malaclemys is completed when terrapins ingest these cysts. At 12 sites along the coast of Georgia (U.S.A.), we determined the prevalence of internal P. malaclemys larvae in mud snails (proportion of infected snails in a population) and the prevalence and mean abundance of external trematode cysts. We examined whether these data were correlated with terrapin abundance, which we estimated with mark-recapture methods. The abundance of external cysts and salinity explained ≥59% of the variability in terrapin abundance. We suggest that dependent linkages between the life stages of multihost parasites make them reliable predictors of host species' abundance, including hosts with abundances that are challenging to quantify directly.

Parasites alter community structure.

Parasites often play an important role in modifying the physiology and behavior of their hosts and may, consequently, mediate the influence hosts have on other components of an ecological community. Along the northern Atlantic coast of North America, the dominant herbivorous snail Littorina littorea structures rocky intertidal communities through strong grazing pressure and is frequently parasitized by the digenean trematode Cryptocotyle lingua. We hypothesized that the effects of parasitism on host physiology would induce behavioral changes in L. littorea, which in turn would modulate L. littorea's influence on intertidal community composition. Specifically, we hypothesized that C. lingua infection would alter the grazing rate of L. littorea and, consequently, macroalgal communities would develop differently in the presence of infected versus uninfected snails. Our results show that uninfected snails consumed 40% more ephemeral macroalgal biomass than infected snails in the laboratory, probably because the digestive system of infected snails is compromised by C. lingua infection. In the field, this weaker grazing by infected snails resulted in significantly greater expansion of ephemeral macroalgal cover relative to grazing by uninfected snails. By decreasing the per-capita grazing rate of the dominant herbivore, C. lingua indirectly affects the composition of the macroalgal community and may in turn affect other species that depend on macroalgae for resources or habitat structure. In light of the abundance of parasites across systems, we suggest that, through trait-mediated indirect effects, parasites may be a common determinant of structure in ecological communities.