The most vagile host as the main determinant of population connectivity in marine macroparasites

Although molecular ecology of macroparasites is still in its infancy, general patterns are beginning to emerge, e.g. that the most vagile host in a complex life cycle is the main determinantof the population genetic structure of their parasites. This insight stems from the observation that populations of parasites with only freshwater hosts are more structured than those with terrestrial or airborne hosts. Until now, the same has not been tested for marine systems, where, in theory, a fully marine life cycle might sustain high dispersal rates because of the absence of Obvious physical barriers in the sea. Here, we tested whether a marine trematode parasite that utilises migratory birds exhibited weaker population genetic structure than those whose life cycle utilises marine fish as the vagile host. Part of the mitochondrial cytochrome c oxidase 1 (COI) gene wassequenced from individual sporocysts from populations along the Atlantic coast of Europe and North Africa. Strong population structure (Φ-ST = 0.25, p < 0.0001) was found in the fully marinetrematode Bucephalus minimus (hosted by fish), while no significant structure (Φ-ST = 0.015, p = 0.19257) was detected in Gymnophallus choledochus (hosted by birds). However, demographicmodels indicate recent colonisation rather than high dispersal as an alternative explanation of the low levels of structure observed in G. choledochus. Our study is the first to identify significant genetic population structure in a marine autogenic parasite, suggesting that connectivity between populations of marine parasites can be limited despite the general potential for high dispersal of their hosts in the marine environment

Biodiversity and bio-evaluation methods in transitional waters: a theoretical challenge

1 - This paper addresses the question of the weaknesses of the methodologies developed based on the analysis of the composition of benthic invertebrate communities in transitional waters.2 - Benthic communities are an important element of the bio-evaluation methodologies suggested for the Ecological Quality status of the European transitional and coastal waters in the context of the Water Framework Directive. It is argued that the assessment of Ecological Quality status requires both fundamental and applied science.3 - The lack of performance of many biotic indices under varying and highly fluctuating environmental conditions may well be related to weakness in theory supporting marine biodiversity.4 - We propose some possible approaches for future development in the field of biotic indices and marine biodiversity theory

Distribution of parasites in their second intermediate host, the cockle Cerastoderma edule: community heterogeneity and spatial scale

We studied the spatial heterogeneity of infection of the marine bivalve Cerastoderma edule (cockle) by trematode parasites at 5 different scales in Banc d'Arguin, France. At the km-scale, the communities of trematodes differed among stations in terms of species composition and specific abundance. Infection heterogeneity was likely due to the occurrence of the definitive host and the conditions of transmission (water parameters). At the 100 m scale, trematode species richness was similar among stations, but specific trematode abundances differed. The most significant variable in terms of explaining trematode infection heterogeneity was the presence of the first intermediate host. At the 10 m scale, the distance at which parasite abundance diminished varied according to trematode species. When an intense source of trematode larvae (cercariae) emission was suspected, this abundance was maintained within ca. 20 m. Outside this area, parasite abundance progressively dropped. We found a higher aggregation in parasite distribution at the 100 m scale than at the 10 m scale using a community aggregation measure. At the cm-scale, the parasite species richness was similar in all cockles but parasite abundance differed in relation to distance when the parasites were shed by a sedentary host compared to a motile host. Observed differences of infection could also be due to intrinsic factors (life history, immune system) as suggested by an experimental infestation where cockles challenged in similar conditions displayed different parasite loads. We demonstrated that high heterogeneity of parasite infection in cockles should be taken into account in studies concerning the role of parasites in ecosystems

Can host density attenuate parasitism?

Bivalve populations display fluctuating densities resulting in different interactions among them and with their environment. Using the edible cockle (Cerastoderma edule) as a model, we investigated two alternative hypotheses concerning the effect of density on individual infection intensity by trematode parasites. Considering that these parasites infect cockles through filtration activity, our first hypothesis was that high host density will have a dilution effect so that infection intensity decreases with host density. Conversely, high cockle density could attract other hosts used by these trematode parasites to complete their life cycle. A 17-year monthly survey of a cockle population in Arcachon Bay, France, showed a negative correlation between the cockle density and the abundance of parasite larvae in juvenile cockles with a significant threshold when adult cockle density reached 400 ind. m−2. This result was confirmed for the four dominating trematode parasites, independently considered. Additionally, a field experiment was performed during 9 months, with cockles maintained in enclosures with two densities (200 and 800 ind. m−2). Individual cockle mean infection was 1.5 times higher at low cockle density, mainly due to one dominant trematode species (Parvatrema minutum). In conclusion and confirming the first advanced hypothesis, for certain environments, negative consequences of bivalve intraspecific competition at high density can be mitigated by lower parasite pressure

Bivalve vulnerability is enhanced by parasites through the deficit of metallothionein synthesis: A field monitoring on cockles (Cerastoderma edule)

The effect of the parasite Labratrema minimus (digenean trematode) on metallothioneins (MTs) biosynthesis by the cockle Cerastoderma edule (bivalve) was investigated. An in situ monitoring allowed to describe and compare monthly variations of MTs concentrations in cockles with and without L. minimus in a site free of metai pollution (Banc d'Arguin, Arcachon Bay, France). These concentrations are correlated with the reproductive cycle of the bivalve: (I) in spent cockles, MTs concentrations are higher in infected cockles. probably due to host tissue lysis: (2) during maturation, MTs biosynthesis increases in all cockles. However, concentrations are lower in parasitized individuals in relation with castration by parasites. Therefore, parasite infection in cockles, which can affect 100% of individuals, may contribute to a higher vulnerability of organisms to metal contamination

Effect of trematode parasites on cockle Cerastoderma edule growth and condition index: a transplant experiment

We quantified the effect of trematode parasites in cockles through a 303 d transplant experiment. Cockles were sampled in 3 different sites on the southwest coast of France characterized by 3 different trematode communities, i.e. Royan (RO): high Meiogymnophallus minutus abundance near cockle heart, South Arguin (SA): high Himasthla interrupta abundance in the mantle margin, and North Arguin (NA): almost free of trematodes. Sampled cockles were individually tagged and placed in different cages at Banc d'Arguin, Arcachon Bay. At the end of the experiment, RO cockles had lost their trematodes, highlighting the fact that trematode lifespan can be short, while SA cockles maintained their trematode load. When cockles were the second intermediate host, there was no effect of site of origin on cockle condition index and survival. The effect on growth rate was mostly due to initial cockle length. Within each treatment, the only significant effect of trematode infection on growth was found for H. interrupta at SA. The 23% growth deficit observed could be due to the disruption of cockle shell synthesis in the mantle margin. During the transplant experiment, cockles were also infected at an exceptionally high rate by Bucephalus minimus, a trematode which invades most of the tissues and uses the cockle as a first intermediate host. Surprisingly, there was an effect on the growth rate and condition index of cockles at only one of the sites under study. This field experiment succeeded in quantifying the moderately negative effect of trematode parasites on the growth and condition of their host and suggested the existence of interactions with as yet unknown factors

Review: bucephalus minimus, a deleterious trematode parasite of cockles Cerastoderma spp.

Trematodes are the most prevalent and abundant macroparasites in coastal waters. They display a complex life cycle with alternation of free-living and parasitic stages generally involving three host species. The most deleterious stage is in the first intermediate host (a mollusc) where the parasite penetrates as miracidium larvae and asexually multiplicates in sporocysts/rediae to provide cercariae larvae. However, due to basic low prevalence in ecosystems, this system remains difficult to study. Taking the example of the cockle (Cerastoderma edule), an exploited bivalve along North- Eastern Atlantic coasts, and Bucephalus minimus, its most prevalent parasite as first intermediate host, we summarised the 51 most relevant papers (1887–2015). Besides, a 16-year monthly monitoring was performed at Banc d’Arguin (Atlantic coast of France), and allowed to obtain a sufficient number of infected cockles (276 out of 5,420 individuals) in order to provide new information concerning this parasite/host system. Sporocysts (diameter 80–500 μm) and developing cercariae (length 300–500 μm) are not visible before cockle reaches 16-mm shell length and then prevalence increases with host size. Seasonality of infection was not observed but variation of prevalence was significant among years and negatively correlated to the temperature of the former year, which could correspond to the period of infection by miracidium. Seven other species of trematode were identified in cockles as second intermediate host. For six of them, metacercariae abundance per individual was 2 to 12 folds higher in B. minimus-infected cockles, exacerbating the potential negative impact on host. From the parasite point of view, metacercariae can be considered as hitchhikers, taking advantage of the abnormalmigration of B. minimus-infected cockles to the sediment surface where they become more vulnerable to predators that are also the final hosts of many of these parasites