High prevalences of disseminated neoplasia in the Baltic tellin Limecola balthica in the Wadden Sea.

The Baltic tellin Limecola balthica is one of the most common bivalves in intertidal areas in the Northern Hemisphere. Over the last 2 decades, the species has been suffering from a decrease in adult survival in the European Wadden Sea. While several factors such as global warming and fisheries have been suggested to influence the population dynamics of this bivalve mollusc, the potential role of diseases has never been investigated. In this study, we investigated whether disseminated neoplasia, a common proliferative disorder in bivalve molluscs, could play a potential role in the recent population decline of Baltic tellins in the Wadden Sea. We conducted a field survey in the Dutch Wadden Sea to (1) determine whether the disease occurs in Baltic tellins in the Wadden Sea and (2) quantify the occurrence and severity of the disease via histology. Disseminated neoplasia occurred in L. balthica at each of the 10 sampled locations with very high prevalences (21-89%) compared to those reported elsewhere for this species. The highest severity category was found in 8 to 87% of affected individuals, with severity generally increasing with prevalence. Disseminated neoplasia usually increases mortality among affected individuals and may also be associated with important sub-lethal effects, especially regarding gametogenesis. Thus, we suggest that disseminated neoplasia may play a key role in the population dynamics of the Baltic tellin, the extent of which remains to be investigated in future studies.

How does the bopyrid isopod Gyge branchialis interfere with trace metal bioaccumulation in the mud shrimp Upogebia cf. pusilla?

Parasites are widespread in natural environments, and their impacts on the fitness of their host and, at a broader scale, on ecosystem functioning are well recognized. Over the last two decades, there has been an increasing interest in the effects of parasites in conjunction with other stressors, especially pollutants, on the health of organisms. For instance, parasites can interfere with the bioaccumulation process of contaminants in their host leading to parasitized organisms exhibiting lower pollutants burdens than unparasitized individuals for example. However, the mechanisms underlying these patterns are not well understood. This study examined how the bopyrid parasite Gyge branchialis could lower the cadmium (Cd) uptake of its mud shrimp host Upogebia cf. pusilla. When exposed to water-borne Cd, parasites were able to bioaccumulate this trace metal. However, the uptake of Cd by the parasite was low and cannot entirely explain the deficit of Cd contamination of the host. The weight of gills of parasitized organisms was significantly reduced compared with unparasitized organisms. We suggest that by reducing the surface for metal uptake, parasites could lower the contaminant burden of their host.

Does parasitism influence sediment stability? Evaluation of trait-mediated effects of the trematode Bucephalus minimus on the key role of cockles Cerastoderma edule in sediment erosion dynamics.

In coastal environments, bioturbators greatly influence the physical and biogeochemical properties of sediments with consequences for central ecological processes such as erosion dynamics. In addition to their direct impact on sediment stability, bioturbators can have an impact on sediment erosion processes by modulating the growth of microphytobenthic organisms that stabilise the surface layer of sediments. The direct and indirect influences of bioturbators on sediment dynamics depend on the magnitude of their activity and inherently on their physiological state. Bioturbators are infected by various parasites, which have a substantial impact on their physiology and behaviour. However, the knock-on effects of parasites on key ecosystem functions like sediment dynamics remain poorly studied. We conducted flume experiments to investigate the indirect influence of the trematode Bucephalus minimus parasitising the common cockle Cerastoderma edule on the dynamics of sandy sediments enriched or not with microphytobenthos (MPB). Cockles modified bed roughness, sediment surface erodibility and hence destabilised sandy sediments. In sediments not enriched with MPB, both unparasitised and parasitised organisms had a similar impact on the stability of sandy sediments. In contrast, parasitism slightly reduced the destabilisation effect of cockles in MPB-enriched sediments. In the latter, parasitised cockles did not interfere with MPB growth whereas unparasitised organisms constrained the microalgae development. However, the enrichment of the surface layers of sandy sediments with MPB did not modulate the erosion dynamics of these environments. Thus, the lower destabilisation effect of parasitised cockles was not here linked to a stabilisation effect of MPB. When standardised for length, parasitised cockles were lighter than unparasitised organisms. Weakened cockles may have had a lower bioturbation potential than unparasitised conspecifics. If so, the influence parasitised cockles had on sediment erodibility and sediment roughness may have been reduced. The absence of a parasitism effect on the dynamics of MPB-unenriched sediments remains nonetheless unclear.

Sediment stability: can we disentangle the effect of bioturbating species on sediment erodibility from their impact on sediment roughness?

Benthic organisms, in particular bioturbators, can influence erosion processes either by affecting sediment roughness through their mere presence and/or activities, or by modulating sediment characteristics (e.g., silt content, granulometry), thus altering its erodibility. To date, it was not possible to distinguish the influence of bioturbating species on sediment roughness from their impact on sediment erodibility. Consequently, uncertainties remain regarding the role played by benthic species on sediment dynamics. In this study, we used a canal flume which allows to record the bed shear stress at the surface of a non-cohesive sediment (4% of mud) during erosion experiments, thus allowing to disentangle the influence of bioturbators, here the common cockle Cerastoderma edule, on the two erosion mechanisms. In order to assess the influence of bioturbators on sediment stability in different environmental situations, we additionally tested for the effects of three factors, i.e. bivalve density, availability of suspended food (i.e. phytoplankton presence) and microphytobenthos (MPB) occurrence, which may modulate the behavior of cockles. We observed that cockles promote the erosion of the sediment surficial layer by increasing its roughness as a consequence of their sediment reworking activity and/or presence at the sediment surface (emerging shell). In contrast, we calculated similar critical bed shear stress for erosion with and without bivalves suggesting that cockles have a minor influence on the erodibility of non-cohesive substrates with a low silt content. The destabilizing effect of cockles increased with the bivalve density whereas it was attenuated by the presence of phytoplankton. We hypothesize that the magnitude of cockles' bioturbation activity was lower when a high proportion of suspended food is available. High concentrations of suspended food may also have enhanced the filtration and biodeposition rates of cockles, thus rapidly leading to the 'muddification' of the sediment bed and consequently counteracting with the own destabilizing effect of the bivalves. Finally, the sole presence of MPB did not significantly affect the resuspension dynamics of non-cohesive sediments with a low proportion of mud.

Seasonal influence of parasitism on contamination patterns of the mud shrimp Upogebia cf. pusilla in an area of low pollution.

Very few studies have characterized the concentrations of pollutants in bioturbating species. These species are considered as ecosystem engineers and characterizing stressors, such as contaminants, that impact them could lead to a better understanding of the functioning of ecosystems. In addition to contaminants, bioturbators are affected by a wide range of stressors, which can influence their physiological status and their ability to accumulate pollutants. Among these stressors, parasitism is of particular concern due to the ubiquity of parasites in natural environments and their influence on the fitness of their host. This study aims to assess the relationship between parasitism and metal accumulation in the bioturbating mud shrimp Upogebia cf. pusilla. A one-year seasonal survey was conducted in Arcachon Bay, France, with the aims of (1) characterizing the levels of metals in the mud shrimp and (2) evaluating the influence of two macroparasites (a bopyrid isopod and a trematode) on the variation of the metal content in mud shrimp. The bopyrid parasite castrates its female host and a particular attention has therefore been paid to the reproductive cycle of female mud shrimp by quantifying the expression of the vitellogenin gene that encodes the major yolk protein in female crustaceans. The levels of contaminants in mud shrimp appeared low compared to those reported in other crustaceans in areas of higher pollution. Even at these low contamination levels, we observed a significant impact by the bopyrid parasite that depends on season: bopyrid-infested organisms are generally more contaminated than their uninfested conspecifics except in summer when the opposite trend was observed. We suggest that the bopyrid indirectly interferes with the metal accumulation process by altering the reproductive capabilities of the mud shrimp. On the opposite, very low influence of the trematode parasite on the metal content of the host was found.

Do trace metal contamination and parasitism influence the activities of the bioturbating mud shrimp Upogebia cf. pusilla?

Mud shrimp are considered as among the most influential ecosystem engineers in marine soft bottom environments because of their significant bioturbation activity and their high density. These organisms play a key role on the physical structure of sediments through intense sediment reworking activity and also deeply influence geochemical properties of sediments via frequent bioirrigation events. The influence that mud shrimp have on the environment is related to the magnitude of bioturbation processes and subsequently depends on their physiological condition. In natural environments, several factors act together and influence the well-being of organisms. Among them, the deleterious role of parasites on the physiology and the behavior of their host is well established. Aquatic organisms are also subject to pollutants released by anthropogenic activities. However, the effect of both stressors on the fitness and bioturbation activity of mud shrimp has never been investigated yet. We conducted a 14-day ex-situ experiment to evaluate the influence of trace metal contamination (cadmium Cd) and parasitism infestation on the gene expression (molecular endpoint) and sediment reworking activity (behavioral endpoint) of the mud shrimp Upogebia cf. pusilla. At completion, mud shrimp exhibited substantial Cd bioaccumulation, with parasitized organisms showing a significantly lower contaminant burden than unparasitized specimens. Cadmium contamination induces modifications of gene expression in both unparasitized and parasitized organisms. We report an antagonistic effect of both stressors on gene expression, which cannot be fully explained by a lower Cd bioaccumulation. At the behaviour level, parasitism seems to reduce the sediment reworking activity of mud shrimp, while Cd contamination appears to stimulate this activity. This study highlights that the effects of multiple stressors may be quite different from the effects of each stressor considered individually. It should also motivate for more studies evaluating the influence of multiple stressors on different endpoints encompassing various levels of organization.

Influence of the bioturbator Upogebia cf. pusilla on trace metal remobilization: Does parasitism matter?

Marine sediments are an important source of contaminants since they are susceptible to be remobilized to the water column. By modifying the physical and biogeochemical characteristics of sediments, bioturbation can influence contaminants remobilization. Within bioturbators, mud shrimp are considered as among the most influential organisms in marine soft-bottom environments. The physiological state of mud shrimp can be impaired by bopyrid parasites. The present study aims to evaluate the influence of bopyrid-uninfested and bopyrid-infested mud shrimp on sediment contaminants resuspension. Through a 14-days ex-situ experiment we showed a moderate effect of mud shrimp on contaminant remobilization compared to molecular diffusion without the bioturbator. Conversely, parasite presence significantly impaired contaminant bioaccumulation in mud shrimp and interfered with genetic expression. The weak effect of mud shrimp on contaminant remobilization may be due to trace metal accumulation and thus we suggested to evaluate the influence of contaminants on activities of bioturbating species.