Consumption of trematode parasite infectious stages: from conceptual synthesis to future research agenda.

Given their sheer cumulative biomass and ubiquitous presence, parasites are increasingly recognized as essential components of most food webs. Beyond their influence as consumers of host tissue, many parasites also have free-living infectious stages that may be ingested by non-host organisms, with implications for energy and nutrient transfer, as well as for pathogen transmission and infectious disease dynamics. This has been particularly well-documented for the cercaria free-living stage of digenean trematode parasites within the Phylum Platyhelminthes. Here, we aim to synthesize the current state of knowledge regarding cercariae consumption by examining: (a) approaches for studying cercariae consumption; (b) the range of consumers and trematode prey documented thus far; (c) factors influencing the likelihood of cercariae consumption; (d) consequences of cercariae consumption for individual predators (e.g. their viability as a food source); and (e) implications of cercariae consumption for entire communities and ecosystems (e.g. transmission, nutrient cycling and influences on other prey). We detected 121 unique consumer-by-cercaria combinations that spanned 60 species of consumer and 35 trematode species. Meaningful reductions in transmission were seen for 31 of 36 combinations that considered this; however, separate studies with the same cercaria and consumer sometimes showed different results. Along with addressing knowledge gaps and suggesting future research directions, we highlight how the conceptual and empirical approaches discussed here for consumption of cercariae are relevant for the infectious stages of other parasites and pathogens, illustrating the use of cercariae as a model system to help advance our knowledge regarding the general importance of parasite consumption.

Biotic and abiotic drivers affect parasite richness, prevalence and abundance in Mytilus galloprovincialis along the Northern Adriatic Sea.

Although it is generally known that a combination of abiotic and biotic drivers shapes the distribution and abundance of parasites, our understanding of the interplay of these factors remains to be assessed for most marine host species. The present field survey investigated spatial patterns of richness, prevalence and abundance of parasites in Mytilus galloprovincialis along the coast of the northern Adriatic Sea. Herein, the relationships between biotic (host size, density and local parasite richness of mussel population) and abiotic (eutrophication and salinity) drivers and parasite richness of mussel individuals, prevalence and abundance were analysed. Local parasite richness was the most relevant factor driving parasite species richness in mussel individuals. Prevalence was mainly driven by eutrophication levels in three out of four parasite species analysed. Similarly, abundance was driven mainly by eutrophication in two parasite species. Mussel size, density and salinity had only minor contributions to the best fitting models. This study highlights that the influence of abiotic and biotic drivers on parasite infections in mussels can be differentially conveyed, depending on the infection measure applied, i.e. parasite richness, prevalence or abundance. Furthermore, it stresses the importance of eutrophication as a major factor influencing parasite prevalence and abundance in mussels in the Adriatic Sea.

Salinity gradient shapes distance decay of similarity among parasite communities in three marine fishes.

Published data were used to compare the distance decay of similarity in parasite communities of three marine fish hosts: Atlantic cod Gadus morhua, the dab Limanda limanda and the flounder Platichthys flesus in two adjacent areas that differ with respect to the strength of a salinity gradient. In the Baltic Sea, which exhibits a strong salinity gradient from its connection with the North Sea in the west to its head in the north-east, parasite communities in all three fish hosts showed a significant decline of similarity with increasing distance. In contrast, among host populations in the North Sea, which is a fully marine environment, there was no such decline or only a weak relationship. The results suggest that environmental gradients like salinity can be strong driving forces behind patterns of distance decay in parasite communities of fishes.

Diversity, decoys and the dilution effect: how ecological communities affect disease risk.

Growing interest in ecology has recently focused on the hypothesis that community diversity can mediate infection levels and disease ('dilution effect'). In turn, biodiversity loss--a widespread consequence of environmental change--can indirectly promote increases in disease, including those of medical and veterinary importance. While this work has focused primarily on correlational studies involving vector-borne microparasite diseases (e.g. Lyme disease, West Nile virus), we argue that parasites with complex life cycles (e.g. helminths, protists, myxosporeans and many fungi) offer an excellent additional model in which to experimentally address mechanistic questions underlying the dilution effect. Here, we unite recent ecological research on the dilution effect in microparasites with decades of parasitological research on the decoy effect in macroparasites to explore key questions surrounding the relationship between community structure and disease. We find consistent evidence that community diversity significantly alters parasite transmission and pathology under laboratory as well as natural conditions. Empirical examples and simple transmission models highlight the diversity of mechanisms through which such changes occur, typically involving predators, parasite decoys, low competency hosts or other parasites. However, the degree of transmission reduction varies among diluting species, parasite stage, and across spatial scales, challenging efforts to make quantitative, taxon-specific predictions about disease. Taken together, this synthesis highlights the broad link between community structure and disease while underscoring the importance of mitigating ongoing changes in biological communities owing to species introductions and extirpations.

Ambient fauna impairs parasite transmission in a marine parasite-host system.

To understand possible factors controlling transmission of trematode larvae between first and second intermediate hosts we examined the impact of ambient fauna on parasite transmission in a marine intertidal parasite-host association. Cockle hosts (Cerastoderma edule) kept together with selected co-occurring macrozoobenthic species in mesocosms acquired a lower parasite load compared to cockles kept alone, when targeted by cercariae of the trematode Himasthla elongata. The reduction of parasite load in the cockles differed between the 7 macrozoobenthic species tested and was between 35 and 91%. Three different types of reduction could be distinguished: (1) predators (Carcinus maenas, Crangon crangon) actively preying upon cercariae, (2) non-host filter feeders (Crepidula fornicata, Mya arenaria, Crassostrea gigas) filtering cercariae but not becoming infected and (3) alternative hosts (Mytilus edulis, Macoma balthica) becoming infected by the cercariae and thus distracting cercariae from the target hosts. In addition, interference competition may occur in the form of disturbance of cockles by ambient organisms resulting in lower filtration rates and subsequently lower parasite loads. Our results suggest that the species composition and relative abundance of the ambient fauna of parasite-host systems play an important role in controlling trematode transmission rates in benthic marine systems.

The role of biotic factors in the transmission of free-living endohelminth stages.

The transmission success of free-living larval stages of endohelminths is generally modulated by a variety of abiotic and biotic environmental factors. Whereas the role of abiotic factors (including anthropogenic pollutants) has been in focus in numerous studies and summarized in reviews, the role of biotic factors has received much less attention. Here, we review the existing body of literature from the fields of parasitology and ecology and recognize 6 different types of biotic factors with the potential to alter larval transmission processes. We found that experimental studies generally indicate strong effects of biotic factors, and the latter emerge as potentially important, underestimated determinants in the transmission ecology of free-living endohelminth stages. This implies that biodiversity, in general, should have significant effects on parasite transmission and population dynamics. These effects are likely to interact with natural abiotic factors and anthropogenic pollutants. Investigating the interplay of abiotic and biotic factors will not only be crucial for a thorough understanding of parasite transmission processes, but will also be a prerequisite to anticipate the effects of climate and other global changes on helminth parasites and their host communities.

Habitat and transmission--effect of tidal level and upstream host density on metacercarial load in an intertidal bivalve.

Transmission of parasites may be mediated by their habitat, consisting of abiotic and biotic components. I investigated the effect of 2 important habitat components in intertidal ecosystems, tidal level (abiotic) and density of upstream hosts (biotic), on the transmission of trematode cercariae to cockle (Cerastoderma edule) hosts. A field survey showed no general trend in metacercarial loads of cockles regarding tidal level but species-dependent reactions. Parasites originating from Littorina littorea (Himasthla elongata, Renicola roscovita) showed highest infection levels in the low intertidal while parasites originating from Hydrobia ulvae (H. continua, H. interrupta) showed highest infection levels in the mid-intertidal. This reflected the density of upstream hosts at both tidal levels and positive relationships between the density of upstream hosts and metacercarial load in cockles suggested the biotic habitat component to be the dominant factor in transmission. This was confirmed by a field experiment, manipulating tidal level and the density of infected upstream snail hosts. While tidal level had no significant effect on the number of metacercariae of H. elongata acquired by cockles, the effect of upstream host density was strong. In conclusion, although tidal level usually is a very important abiotic habitat component in intertidal ecosystems leading to conspicuous zonation patterns in free-living organisms, it seems of minor importance for trematode transmission. In contrast, the biotic component upstream host density is suggested to be the dominant predictor for trematode transmission to second intermediate hosts. Assessing the relative importance of abiotic and biotic habitat components in transmission is vital for the understanding of transmission processes in the field.