Temporal Community Structure in Two Gregarines (Rotundula gammari and Heliospora longissima) Co-Infecting the Amphipod Gammarus fasciatus.

This study surveyed gregarine parasites that infect the amphipod, Gammarus fasciatus , to investigate temporal dynamics in infracommunity structure. We sampled a population of hosts for 2 yr from the north branch of the Raritan River in New Jersey. These hosts were infected with 2 direct life cycle gregarine parasites, Rotundula gammari and Heliospora longissima. Infections were separated temporally, with the prevalence of R. gammari peaking within the amphipod population in the fall (prevalence = 78% year 1 and 97% year 2) and H. longissima peaking in early spring (prevalence = 41% year 1 and 52% year 2). Increases in host population density did not significantly correlate with the abundance of these 2 parasites. However, H. longissima abundance was positively correlated with host body weight while R. gammari showed no significant relationship. The mean body mass of amphipods infected with H. longissima was 20.7 ± 1. 2 mg, and with R. gammari 8.1 ± 0.2 mg, which suggests a sized-based infection pattern. Mixed species infections were infrequent with an overall prevalence of 4.6%. When both gregarine species co-infected the same host, the R. gammari but not the H. longissima infrapopulation size was significantly lower when compared to single-species infections, suggesting asymmetric interactions. We conclude that the observed temporal patterns of infection by the 2 parasites are driven by a seasonal change in host demographics and size-dependent infections. We argue that specificity for host developmental stages may have arisen as a mechanism to avoid overlap between these gregarine species.

Habitat-based constraints on food web structure and parasite life cycles.

Habitat is frequently implicated as a powerful determinant of community structure and species distributions, but few studies explicitly evaluate the relationship between habitat-based patterns of species' distributions and the presence or absence of trophic interactions. The complex (multi-host) life cycles of parasites are directly affected by these factors, but almost no data exist on the role of habitat in constraining parasite-host interactions at the community level. In this study the relationship(s) between species abundances, distributions and trophic interactions (including parasitism) were evaluated in the context of habitat structure (classic geomorphic designations of pools, riffles and runs) in a riverine community (Raritan River, Hunterdon County, NJ, USA). We report 121 taxa collected over a 2-year period, and compare the observed food web patterns to null model expectations. The results show that top predators are constrained to particular habitat types, and that species' distributions are biased towards pool habitats. However, our null model (which incorporates cascade model assumptions) accurately predicts the observed patterns of trophic interactions. Thus, habitat strongly dictates species distributions, and patterns of trophic interactions arise as a consequence of these distributions. Additionally, we find that hosts utilized in parasite life cycles are more overlapping in their distributions, and this pattern is more pronounced among those involved in trophic transmission. We conclude that habitat structure may be a strong predictor of parasite transmission routes, particularly within communities that occupy heterogeneous habitats.

Qualitative community stability determines parasite establishment and richness in estuarine marshes.

The establishment of parasites with complex life cycles is generally thought to be regulated by free-living species richness and the stability of local ecological interactions. In this study, we test the prediction that stable host communities are prerequisite for the establishment of complex multi-host parasite life cycles. The colonization of naïve killifish, Fundulus heteroclitus, by parasites was investigated in 4 salt marsh sites that differed in time since major ecological restoration, and which provided a gradient in free-living species richness. The richness of the parasite community, and the rate at which parasite species accumulated in the killifish, were similar between the low diversity unrestored site and the two high diversity (10- and 20-year) restored marsh sites. The parasite community in the newly restored marsh (0 year) included only directly-transmitted parasite species. To explain the paradox of a low diversity, highly invaded salt marsh (unrestored) having the same parasite community as highly diverse restored marsh sites (10 and 20 yrs) we assessed qualitative community stability. We find a significant correlation between system stability and parasite species richness. These data suggest a role for local stability in parasite community assembly, and support the idea that stable trophic relationships are required for the persistence of complex parasite life cycles.

The relationship between community species richness and the richness of the parasite community in Fundulus heteroclitus.

This study examined the relationship between the metazoan parasite community in a focal species, Fundulus heteroclitus , and the species richness of the free-living community. Four distinct salt marsh areas were selected in order to reflect a gradient in free-living species richness and time post-restoration (unrestored, 0, 10, and 20 yr post-restoration). A total of 960 fish was studied, with 30 collected per site in each of 8 consecutive seasons between 2005 and 2007. Species richness and abundance of birds, fish, and benthic macroinvertebrates varied significantly between sites. However, increasing richness in the free-living community was neither positively nor negatively correlated with richness in the parasite infracommunity in F. heteroclitus . These results demonstrate that the relationship between community species richness and parasite richness is not linear. The data suggest that the diversity of parasites may be more correlated with measures of community composition, such as the structure and cohesiveness of the food web, rather than with prevailing measures of biodiversity.

Where are the parasites in food webs?

This review explores some of the reasons why food webs seem to contain relatively few parasite species when compared to the full diversity of free living species in the system. At present, there are few coherent food web theories to guide scientific studies on parasites, and this review posits that the methods, directions and questions in the field of food web ecology are not always congruent with parasitological inquiry. For example, topological analysis (the primary tool in food web studies) focuses on only one of six important steps in trematode life cycles, each of which requires a stable community dynamic to evolve. In addition, these transmission strategies may also utilize pathways within the food web that are not considered in traditional food web investigations. It is asserted that more effort must be focused on parasite-centric models, and a central theme is that many different approaches will be required. One promising approach is the old energetic perspective, which considers energy as the critical resource for all organisms, and the currency of all food web interactions. From the parasitological point of view, energy can be used to characterize the roles of parasites at all levels in the food web, from individuals to populations to community. The literature on parasite energetics in food webs is very sparse, but the evidence suggests that parasite species richness is low in food webs because parasites are limited by the quantity of energy available to their unique lifestyles.

Host quality and spatial patterning in infections of the Eastern mudsnail (Ilyanassa obsoleta) by two trematodes (Himasthla quissetensis and Zoogonus rubellus).

Several studies have suggested that the fitness of a parasite can be directly impacted by the quality of its host. In such cases, selective pressures could act to funnel parasites towards the highest-quality hosts in a population. The results of this study demonstrate that snail host quality is strongly correlated with spatial patterning in trematode infections and that habitat type is the underlying driver for both of these variables. Two trematodes (Himasthla quissetensis and Zoogonus rubellus) with very different life cycles assume the same spatial infection pattern in populations of the first intermediate host (Ilyanassa obsoleta) in coastal marsh habitats. Infected snails are disproportionately recovered from intertidal panne habitats, which offer more hospitable environs for snails than do adjacent habitats (intertidal creeks, coastal flats, and subtidal creeks), in terms of protection from turbulence and wave action, as well as the availability of food stuffs. Snails in intertidal panne habitats are of higher quality when assessed in terms of average size-specific mass, growth rate, and fecundity. In mark-recapture experiments, snails frequently dispersed into intertidal pannes but were never observed leaving them. In addition, field experiments demonstrate that snails confined to intertidal panne habitats are disproportionately infected by both trematode species, relative to conspecifics confined to adjacent habitats. Laboratory experiments show that infected snails suffer significant energetic losses and consume more than uninfected conspecifics, suggesting that infected snails in intertidal pannes may survive better than in adjacent habitats. We speculate that 1 possible mechanism for the observed patterns is that the life cycles of both trematode species allows them to contact the highest-quality snails in this marsh ecosystem.

The roles of mosquito and bird communities on the prevalence of West Nile virus in urban wetland and residential habitats.

This study investigated the impacts of urban wetlands and their adjacent residential environments on the transmission dynamics of West Nile virus (WNV) within the state of New Jersey (USA). A working hypothesis was that urban wetlands decrease the local prevalence of WNV through the dilution effect from increased bird diversity, and through relative reductions in the numbers of competent avian host and mosquito species commonly associated with WNV. Surveys of mosquito and bird communities were undertaken at six urban wetlands and their adjacent residential environments over two seasons (2009, 2010). The community compositions of both avian and mosquito species differed significantly across habitats, and over relatively short geographical distances. Residential areas contained significantly higher proportions of WNV-competent mosquito species (31.25±5.3 %; e.g. Culex pipiens and Culex restuans), and WNV-competent avian host species (62.8±2.3 %, e.g. House Sparrow and American Robin) when compared to adjacent urban wetlands (13.5±2.1 %; 35.4±2.1 % respectively). Correspondingly, WNV infection rates within local Culex spp. populations indicate that WNV was more prevalent within residential areas (28.53/1000) compared to wetlands (16.77/1000). Large urban wetlands (>100 ha) produced significantly lower weekly WNV infection rates in local Culex spp. (6.67±2.84/1000) compared to small (<15 ha) wet-lands (22.57±6.23/1000). Avian species richness was also influenced by patch size. Large urban wetlands contained significantly more species than small wetland patches. These results confirm that the community compositions of mosquito and avian hosts are important drivers in WNV infections, and that the ecological conditions that favor transmission are more strongly associated with urban residential environments than with adjacent urban wetlands.

Host centrality in food web networks determines parasite diversity.

BACKGROUND: Parasites significantly alter topological metrics describing food web structure, yet few studies have explored the relationship between food web topology and parasite diversity. METHODS/PRINCIPAL FINDINGS: This study uses quantitative metrics describing network structure to investigate the relationship between the topology of the host food web and parasite diversity. Food webs were constructed for four restored brackish marshes that vary in species diversity, time post restoration and levels of parasitism. Our results show that the topology of the food web in each brackish marsh is highly nested, with clusters of generalists forming a distinct modular structure. The most consistent predictors of parasite diversity within a host were: trophic generality, and eigenvector centrality. These metrics indicate that parasites preferentially colonise host species that are highly connected, and within modules of tightly interacting species in the food web network. CONCLUSIONS/SIGNIFICANCE: These results suggest that highly connected free-living species within the food web may represent stable trophic relationships that allow for the persistence of complex parasite life cycles. Our data demonstrate that the structure of host food webs can have a significant effect on the establishment of parasites, and on the potential for evolution of complex parasite life cycles.

Food webs for parasitologists: a review.

This review examines the historical origins of food web theory and explores the reasons why parasites have traditionally been left out of food web studies. Current paradigms may still be an impediment because, despite several attempts, it remains virtually impossible to retrofit parasites into food web theory in any satisfactory manner. It seems clear that parasitologists must return to first principles to solve how best to incorporate parasites into ecological food webs, and a first step in changing paradigms will be to include parasites in the classic ecological patterns that inform food web theory. The limitations of current food web models are discussed with respect to their logistic exclusion of parasites, and the traditional matrix approach in food web studies is critically examined. The well-known energetic perspective on ecosystem organization is presented as a viable alternative to the matrix approach because it provides an intellectually powerful theoretical paradigm for generating testable hypotheses on true food web structure. This review proposes that to make significant contributions to the food web debate, parasitologists must work from the standpoint of natural history to elucidate patterns of biomass, species abundance, and interaction strengths in real food webs, and these will provide the basis for more realistic models that incorporate parasite dynamics into the overall functional dynamics of the whole web. A general conclusion is that only by quantifying the effects of parasites in terms of energy flows (or biomass) will we be able to correctly place parasites into food webs.

Parasites alter the topology of a stream food web across seasons.

Relatively few published food webs have included parasites, and in this study we examined the animal community in a stream across eight contiguous seasons to test how inclusion of helminth parasites alters the topology or structure of the food web. Food webs constructed for each season and analyzed using common binary matrix measures show that species richness, linkage density, and the number of observed and possible links increased when parasites were included as individual species nodes. With parasite-parasite and predator-parasite links omitted, measures of community complexity, such as connectance (C), generally increased over multiple seasons. However, relative nestedness (n*) decreased when parasites were included, which may be a result of low resolution of basal resources inflating specialist-to-specialist links. Overall, adding parasites resulted in moderate changes in food web measures when compared to those of four other published food webs representing different ecosystems. In addition, including parasites in the food web revealed consistent pathways of energy flow, and the association of parasite life histories along these pathways suggest stable evolutionary groups of interacting species within the community.

Parasite effects on isopod feeding rates can alter the host's functional role in a natural stream ecosystem.

Changes to host behaviour as a consequence of infection are common in many parasite-host associations, but their effects on the functional role hosts play within ecosystems are rarely quantified. This study reports that helminth parasites significantly decrease consumption of detritus by their isopod hosts in laboratory experiments. Natural host and parasite densities across eight contiguous seasons were used to estimate effects on the amount of stream detritus-energy processed. Extrapolations using mass-specific processing rates from laboratory results to field patterns suggest that the effects of the parasites occur year round but the greatest impact on the amount of detritus processed by isopods occurs in the autumn when the bulk of leaf detritus enters the stream, and when parasite prevalence in the isopod population is high. Parasites have a lesser impact on the amount of detritus processed in spring and summer when isopods are most abundant, when parasite prevalence is not high, and when fish predation on isopods is high. These results support the idea that parasites can affect the availability of resources critical to other species by altering behaviours related to the functional role hosts play in ecosystems, and suggest that seasonality may be an important factor to consider in the dynamics of these parasite-host interactions.