In a range of trematode species, specific members of the parthenitae colony infecting the molluscan first intermediate host appear specialized for defence against co-infecting species. The evolution of such division of labour requires that co-infection entails fitness costs. Yet, this premise has very rarely been tested in species showing division of labour. Using Himasthla elongata (Himasthlidae) and Renicola roscovita (Renicolidae) infecting periwinkles Littorina littorea as study system, we show that the size of emerged cercariae is markedly reduced in both parasite species when competing over host resources. Cercarial longevity, on the other hand, is negatively influenced by competition only in R. roscovita. Season, which may impact the nutritional state of the host, also affects cercarial size, but only in H. elongata. Hence, our study underlines that cercarial quality is, indeed, compromised by competition, not only in the inferior R. roscovita (no division of labour) but also in the competitively superior H. elongata (division of labour).

Digenean larvae of hermaphroditic generation – cercariae – are known to be polymorphic at genetic and behavioural levels. Cercariae arise as a result of parthenogenetic reproduction of intramolluscan stages, and represent a clone if a snail was infected with a single miracidium. Here we investigated cercarial clones of Himasthla elongata – namely, the infectivity of cercariae with normal (negative) and deviant (positive) photoreaction. In our study, most H. elongata clones showed intraclonal variance in their response to light. The proportion of photopositive cercariae ranged between 0.2% and 60% in different H. elongata clones. Photopositive larvae demonstrated significantly reduced rates of encystment in Mytilus edulis haemolymph in vitro and in young mussels. We discuss the possible mechanisms behind intraclonal variations, such as non-specific genomic rearrangements.

Parasites competing over limited host resources are faced with a tradeoff between reproductive success and host overexploitation jeopardizing survival. Surprisingly little is known about the outcome of such competitive scenarios, and we therefore aimed at elucidating interactions between the trematodes Himasthla elongata and Renicola roscovita coinfecting the periwinkle first intermediate host. The results show that the success of Himasthla colonies (rediae) in terms of cercarial emission is unaffected by Renicola competition (sporocysts), whereas deteriating host condition decreases fitness. Furthermore, double infection has no bearing on Himasthla’s colony size but elevated the proportion of non-reproductive rediae that play a decisive role in colony defence. Opposite, the development of the Renicola colony (size/maturity), and in turn fitness, is markedly reduced in presence of Himasthla, whereas the nutritional state of the host appears less important. Hence, the intramolluscan competition between Himasthla and Renicola is asymmetrical, Himasthla being the superior competitor. Himasthla not only adjusts its virulence according to the hosts immediate nutritional state, it also nullifies the negative impact of a heterospecific competitor on own fitness. The latter is argued to follow in part from direct predation on the competitor, for which purpose more defensive non-reproductive rediae are strategically produced.

Reproductive division of labour is well-known in several animal groups but the ecological factors driving the evolution of such social organization are still being discussed. Recent studies have discovered social organization in four marine species of trematode parasites having two distinct castes specialized for reproduction and defence of the clonal intra-molluscan larval colony, respectively. Here, we provide novel evidence for social structure also in colonies of the trematode Himasthla elongata infecting the common periwinkle Littorina littorea. We found two types of rediae, the parthenogenetic larval offspring of the parasite: small non-reproductive rediae and considerably larger reproductive rediae. Both redial types possessed a digestive system, collar and posterior appendages and, hence, aside from dimensions, were morphologically similar. However, in vitro experiments showed that non-reproductive morphs attacked heterospecific competing parasites at a higher rate (2–3 fold) than reproductive morphs did. No within-colony antagonism was observed. In contrast to a previous study on a congeneric trematode species, our findings suggest a relatively weak caste formation in H. elongata, possibly resulting from a corresponding weaker level of interspecific competition.

It has increasingly been recognized that organisms can interfere with parasitic free-living stages, preventing them from infecting their specified host and thus reducing infection levels. This common phenomenon in freshwater and terrestrial systems has been termed the ‘dilution effect’ and, so far, is poorly studied in marine systems. Ten common intertidal organisms found in the Dutch Wadden Sea (North Sea) were tested to establish their effects on the free-living cercarial stages of the trematode parasite Himasthla elongata. Most species tested resulted in a significant reduction in cercariae over a 3 hr time period. The amphipod Gammarus marinus removed 100% of the cercariae, while other effective diluters were Crangon crangon (93%), Sargassum muticum (87%), Semibalanus balanoides (71%), Crassostrea gigas (67%), Hemigrapsus takanoi (>54%), Crassostrea gigas shells (44%) and Idotea balthica (24%). In contrast, mixed shells (Cerastoderma edule, Mytilus edulis, Ensis americanus and Littorina littorea) and Fucus versiculosus had no significant effect. These results suggest that dilution effects are widespread in the trematode of H. elongata, with potentially strong effects on its population dynamics.

Trematodes are ubiquitous elements of coastal ecosystems that commonly modify the phenotype of their invertebrate hosts, often with ramifications to higher levels of ecological organization. In this context, trematode infections have been suggested to reduce the consumption of the herbivorous gastropod Littorina littorea (L.) (Mollusca: Gastropoda), in turn affecting the composition of the macroalgal community on which the snail grazes. Here, we examine the effect of two species of trematodes, Renicola roscovita and Himasthla elongata, on L. littorea's consumption in two outdoor microcosm experiments offering the snails two different ephemeral green algae species as a food source. Our results show that, irrespective of the species of parasite and food source, infection decreases consumption: uninfected snails consumed up to 65% more macroalgal biomass than infected snails. Aside from infection status, gender and size also influenced the snails' consumption rate significantly. The differing histopathological impacts of the two species of trematodes on the hosts' gonad–digestive gland complex (in which the parasites reside), suggests that parasitic castration is a likely mechanism for the reduced energy demand of infected periwinkles. Together with existing evidence, our investigation suggests that trematodes in general depress the grazing activity of L. littorea, and that the resulting community regulation occurs throughout the snails' distributional range.

The aim of the present study was to analyse the relation between parasitism and subsequent metallothioneins (MT) in the case of metal contamination. Experimental exposure of parasitized and unparasitized cockles (Cerastoderma edule) to cadmium (Cd) was performed, with the cockle as first or second intermediate host of 2 digenean species. After 7 days of Cd exposure in microcosms, cockles infected as first intermediate host by Labratrema minimus exhibited metal concentrations in tissues double that in uninfected cockles. Jointly, MT concentrations of parasitized cockles were not modified in comparison with uninfected individuals in which concentrations were increased 4·3-fold compared with controls. In cockles experimentally infected as the second intermediate host by Himasthla elongata, cadmium concentrations significantly increased again in parasitized cockles compared with uninfected individuals in contaminated conditions. Simultaneously, MT concentrations in healthy cockles increased, whereas they significantly decreased in parasitized individuals. Therefore, the presence of digenean parasites in Cd-exposed cockles leads to a maintenance or a decrease in MT concentrations compared with healthy individuals, whereas Cd accumulation in tissues is significantly increased. These experiments indicate a significant alteration of the protective effect of metallothioneins towards metals which could consequently enhance cockle vulnerability. Moreover, these results highlight the limit of the use of MT as a biomarker of metal pollution in field monitoring if parasitism is not taken into account.