Invasive oysters as new hosts for native shell-boring polychaetes: Using historical shell collections and recent field data to investigate parasite spillback in native mussels in the Dutch Wadden Sea

Biological invasions can have manifold effects on native biota, including impacts on species interactions in invaded ecosystems. Among those are effects on parasite-host interactions, for example in cases where invaders serve as a new host for native parasites, leading to an amplification of the parasite population which may ultimately result in increased infection levels in the original native hosts (parasite spillback). In this study, we investigated the potential spillback of the native shell-boring polychaete Polydora ciliata from invasive Pacific oysters (Crassostrea (Magallana) gigas) to native mussels (Mytilus edulis) in the Dutch Wadden Sea. A field survey in the intertidal revealed that the majority of P. ciliata can nowadays be found in the shells of live but also dead Pacific oysters and much less in shells of other potential host species: mussels and periwinkles (Littorina littorea). Using a unique historical shell collection based on long-term sampling programmes in the intertidal and subtidal of the western Dutch Wadden Sea, we compared P. ciliata infections in mussels before and after the invasion of the Pacific oyster by means of x-ray scans. Both for the intertidal and subtidal, we did not detect differences in prevalence of P. ciliata in mussels between pre- and post-invasion periods. This suggests that the invasion of the Pacific oyster may not have caused a strong spillback to mussels regarding P. ciliata and thus the invasion probably had little indirect infection-mediated effects on the condition and fitness of native mussels. Instead, the acquisition of native P. ciliata by the invasive oysters suggests that they may themselves be affected by the new infections and this may warrant further research

Freshening rather than warming drives trematode transmission from periwinkles to mussels

In the Western Baltic Sea, climate change is happening at much faster rate than in most other seas and organisms are additionally exposed to a steep and variable salinity gradient. Climate change has previously been shown to affect parasite transmission in other marine ecosystems, yet little is known about potential effects of warming and desalination on parasite–host interactions. In laboratory experiments, we determined the combined effects of projected seawater warming and freshening on the emergence, activity, survival, and infectivity of cercariae (free-swimming infectious stage) of the trematode Himasthla elongata (Mehlis 1831), shed from its first intermediate host, the periwinkle Littorina littorea (Linnaeus 1758), in the Baltic Sea. We also assessed the susceptibility of the second intermediate host, the mussel Mytilus edulis Linnaeus, 1758, to cercarial infections. Generally, salinity was the main driver, particularly of cercarial activity, infectivity, and mussel susceptibility to infection. At the lowest salinity (13), cercariae were 50% less active compared to the highest salinity (19). Infection success and host susceptibility followed a similar pattern, with 47% and 43% less metacercariae (encysted stage) present at salinity 13 than at salinity 19, respectively. In contrast, effects of simulated warming were found only for cercarial survival, with cercarial longevity being higher at 19 than at 23 °C. No significant interactions between temperature and salinity were found. In contrast to the literature, the results suggest that a climate change-driven freshening (partly also warming) may lead to a general decline of marine trematodes, with possible beneficial effects for the involved hosts

Biological invasions and host–parasite coevolution: different coevolutionary trajectories along separate parasite invasion fronts

Host–parasite coevolution has rarely been observed in natural systems. Its study often relies on microparasitic infections introducing a potential bias in the estimation of the evolutionary change of host and parasite traits. Using biological invasions as a tool to study host–parasite coevolution in nature can overcome these biases. We demonstrate this with a cross-infection experiment in the invasive macroparasite <i>Mytilicola intestinalis</i> and its bivalve host, the blue mussel <i>Mytilus edulis</i>. The invasion history of the parasite is well known for the southeastern North Sea and is characterised by two separate invasion fronts that reached opposite ends of the Wadden Sea (i.e. Texel, The Netherlands and Sylt, Germany) in a similar time frame. The species’ natural history thus makes this invasion an ideal natural experiment to study host–parasite coevolution in nature. We infected hosts from Texel, Sylt and Kiel (Baltic Sea, where the parasite is absent) with parasites from Texel and Sylt, to form sympatric, allopatric and naïve infestation combinations, respectively. We measured infection rate, host condition and parasite growth to show that sympatric host–parasite combinations diverged in terms of pre- and post-infection traits within <100 generations since their introduction. Texel parasites were more infective and more efficient at exploiting the host’s resources. Hosts on Texel, on the other hand, evolved resistance to infection, whereas hosts on Sylt may have evolved tolerance. This illustrates that different coevolutionary trajectories can evolve along separate invasion fronts of the parasite, highlighting the use of biological invasions in studies of host–parasite coevolution in nature

Spread of the invasive shell-boring annelid Polydora websteri (Polychaeta, Spionidae) into naturalised oyster reefs in the European Wadden Sea

With globally growing aquaculture activities, the co-introduction of parasites alongside large-scale movements of commercial species poses an increasing risk for marine ecosystems. Here, we present the first record of the shell-boring polychaete Polydora websteri Hartman in Loosanoff and Engle, 1943 in invasive Pacific oysters Crassostrea (Magallana) gigas (Thunberg, 1793) in the European Atlantic Ocean. In October 2014, mud blisters in the shells of wild Pacific oysters and specimens of a spionid polychaete were observed in close proximity to a commercial oyster farm at the island of Sylt (Germany) in the European Wadden Sea. Subsequent investigations indicated that these blisters only occurred near the farm and that no other mollusc species were affected. Morphological and molecular analysis identified the polychaete as Polydora websteri, a species that nowadays widely occurs around the globe, but likely is native to the Asian Pacific. Later sampling activities detected P. websteri also at other locations around Sylt as well as in the Dutch part of the Wadden Sea at the island of Texel. The number of polychaetes in the oysters was, however, relatively low and mostly below 10 individuals per oyster. Together, this evidence suggests that P. websteri is currently extending its range. As the introduction of P. websteri may have severe ecological and economic implications, this study aims to alert others to look for P. websteri at Western European coasts within farmed or wild Pacific oysters to further document its spread

Cryptic invasion of a parasitic copepod: Compromised identification when morphologically similar invaders co-occur in invaded ecosystems

Despite their frequent occurrence and strong impacts on native biota, biological invasions can long remain undetected. One reason for this is that an invasive species can be morphologically similar to either native species or introduced species previously established in the same region, and thus be subject to mistaken identification. One recent case involves congeneric invasive parasites, copepods that now infect bivalve hosts along European Atlantic coasts, after having been introduced independently first from the Mediterranean Sea (Mytilicola intestinalis Steuer, 1902) and later from Japan (Mytilicola orientalis Mori, 1935). At least one report on M. intestinalis may have actually concerned M. orientalis, and M. orientalis thus qualifies as a "cryptic invader". Because these two parasitic copepods are morphologically similar, knowledge about their distribution, impact and interactions depends crucially on reliable species identification. In this study, we evaluated the reliability of morphological identification of these two species in parts of their invasive range in Europe (Dutch Delta and Wadden Sea) in comparison with molecular methods of well-established accuracy based on COI gene sequences and ITS1 restriction fragment length polymorphism. Based on seven easily measured or scored macro-morphological variables that were recorded for 182 individual copepods isolated from blue mussels (Mytilus edulis Linnaeus, 1758), principal component analysis showed two relatively distinct but overlapping morphological species groups for females, but no clear separation in males. Discriminant function analysis showed that the females can be discriminated reasonably well based on some of the morphological characteristics (identification error rate of 7%) while males cannot (error rate of 25%). The direction of the dorsolateral thoracic protuberances was identified as the most important trait for species discrimination, but among the morphological features checked, none could flawlessly discriminate between both species. We recommend the use of molecular techniques in future studies of invasive Mytilicola to reliably discriminate between the species. The morphological similarity of these two invaders suggests a more general problem of cryptic invasions and compromised identification of parasites in invaded ecosystems. This problem should be borne in mind whenever invasive parasites are investigated

First record of the endoparasitic isopod Portunion maenadis (Giard, 1886) (Epicaridea: Entoniscidae) in shore crabs in the Wadden Sea and a review of its distribution in Europe

The knowledge on the distribution and abundance of marine parasites is still limited, even for those occurring on relatively well studied host species with high ecological importance. Here we report on the first record of the entoniscid Portunion maenadis (Giard, 1886) in European shore crabs ( Carcinus maenas L., 1758) in the Wadden Sea and provide a quantitative review of the parasite's distribution in Europe based on published literature and biodiversity database records. Our new record closes a distribution gap of P. maenadis between previous southern observations in Portugal and France and northern occurrences in Denmark and Sweden. The additional literature survey suggests that P. maenadis is not very common and only occurs at scattered localities with prevalence of infestations usually well below 10% in host crab populations. However, the 45% prevalence observed in our study in November 2018 in the southern Wadden Sea indicates that also higher prevalences can occur. As the adult parasites feed on their host’s hemolymph they are likely to have consequences for the host`s energy budgets. In addition, infestations lead to morphological changes in the form of feminisation of male crabs (i.e. broader pleon, slender claws, bulging carapace) which we observed in several individuals. With this new record and literature review we hope to spark future research into the distribution of this intriguing parasite species as well as on the impacts of infestations on shore crab hosts

Spatial and Temporal Dynamics of Pacific Oyster Hemolymph Microbiota across Multiple Scales

Unveiling the factors and processes that shape the dynamics of host associated microbial communities (microbiota) under natural conditions is an important part of understanding and predicting an organism's response to a changing environment. The microbiota is shaped by host (i.e., genetic) factors as well as by the biotic and abiotic environment. Studying natural variation of microbial community composition in multiple host genetic backgrounds across spatial as well as temporal scales represents a means to untangle this complex interplay. Here, we combined a spatially-stratified with a longitudinal sampling scheme within differentiated host genetic backgrounds by reciprocally transplanting Pacific oysters between two sites in the Wadden Sea (Sylt and Texel). To further differentiate contingent site from host genetic effects, we repeatedly sampled the same individuals over a summer season to examine structure, diversity and dynamics of individual hemolymph microbiota following experimental removal of resident microbiota by antibiotic treatment. While a large proportion of microbiome variation could be attributed to immediate environmental conditions, we observed persistent effects of antibiotic treatment and translocation suggesting that hemolymph microbial community dynamics is subject to within-microbiome interactions and host population specific factors. In addition, the analysis of spatial variation revealed that the within-site microenvironmental heterogeneity resulted in high small-scale variability, as opposed to large-scale (between-site) stability. Similarly, considerable within-individual temporal variability was in contrast with the overall temporal stability at the site level. Overall, our longitudinal, spatially-stratified sampling design revealed that variation in hemolymph microbiota is strongly influenced by site and immediate environmental conditions, whereas internal microbiome dynamics and oyster-related factors add to their long-term stability. The combination of small and large scale resolution of spatial and temporal observations therefore represents a crucial but underused tool to study host-associated microbiome dynamics

Lessepsian migration and parasitism: richness, prevalence and intensity of parasites in the invasive fish Sphyraena chrysotaenia compared to its native congener Sphyraena sphyraena in Tunisian coastal waters

Background Parasites can play various roles in the invasion of non-native species, but these are still understudied in marine ecosystems. This also applies to invasions from the Red Sea to the Mediterranean Sea via the Suez Canal, the so-called Lessepsian migration. In this study, we investigated the role of parasites in the invasion of the Lessepsian migrant Sphyraena chrysotaenia in the Tunisian Mediterranean Sea. Methods We compared metazoan parasite richness, prevalence and intensity of S. chrysotaenia (Perciformes: Sphyraenidae) with infections in its native congener Sphyraena sphyraena by sampling these fish species at seven locations along the Tunisian coast. Additionally, we reviewed the literature to identify native and invasive parasite species recorded in these two hosts. Results Our results suggest the loss of at least two parasite species of the invasive fish. At the same time, the Lessepsian migrant has co-introduced three parasite species during the initial migration to the Mediterranean Sea, that are assumed to originate from the Red Sea of which only one parasite species has been reported during the spread to Tunisian waters. In addition, we found that the invasive fish has acquired six parasite species that are native in the Mediterranean Sea. However, parasite richness, prevalence and intensity were overall much lower in the invasive compared to the native fish host in the Mediterranean Sea. Discussion These results suggest that the Lessepsian migrant may affect native fish hosts by potentially altering the dynamics of native and invasive parasite-host interactions via parasite release, parasite co-introduction and parasite acquisition. They further suggest that the lower infection levels in the invasive fish may result in a competitive advantage over native fish hosts (enemy release hypothesis). This study demonstrates that cross-species comparisons of parasite infection levels are a valuable tool to identify the different roles of parasites in the course of Lessepsian migrations

Collateral diseases: Aquaculture impacts on wildlife infections

Aquaculture is a promising source of fish and other aquatic organisms to ensure human food security but it comes at the price of diverse environmental impacts. Among others, these include diseases which often thrive under the conditions in aquaculture settings and can cause high economic losses. These diseases may also affect wildlife, however, the impacts of aquaculture on disease dynamics in wild species in surrounding ecosystems are poorly understood. In this Review, we provide a conceptual framework for studying the effects of aquaculture on wildlife diseases, and illustrate the different mechanisms identified with examples from the literature. In addition, we highlight further research needs and provide recommendations for management and policy. We identified five potential means by which farmed populations may alter wildlife disease dynamics: (a) farmed species may co-introduce parasites to the new environment, which infect wild conspecifics without infecting other species (intraspecific parasite spillover); (b) these co-introduced parasites from farmed species may infect other wild host species potentially leading to emerging diseases (interspecific parasite spillover); (c) parasites from other wild host species may infect farmed species, amplifying parasite numbers and increasing parasite infections when spilling back to wild hosts (interspecific parasite spillback); (d) farmed species may acquire parasites from wild conspecifics, increasing parasite population size and subsequently raising infection loads in the wild host population (intraspecific parasite spillback); and (e) farmed species may be neither hosts nor parasites, but affect the transmission of parasites between wild host species (transmission interference). Although these mechanisms can alter wildlife disease dynamics, we found large knowledge gaps regarding collateral disease impacts and strong biases in terms of production countries, aquaculture practices and host taxa. Synthesis and applications. The strong potential for aquaculture to affect the dynamics of diseases in wildlife populations calls for the consideration of collateral disease impacts in risk assessments and biosecurity protocols regarding aquaculture. In particular, comprehensive parasite inventories of both farmed and wild hosts as well as disease monitoring in wildlife surrounding farms will be necessary to increase our knowledge on aquaculture impacts on wildlife disease and to develop adequate prevention and mitigation measures. © 2020 The Authors. Journal of Applied Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Societ

Parasite avoidance behaviours in aquatic environments

Parasites, including macroparasites, protists, fungi, bacteria and viruses, can impose a heavy burden upon host animals. However, hosts are not without defences. One aspect of host defence, behavioural avoidance, has been studied in the terrestrial realm for over 50 years, but was first reported from the aquatic environment approximately 20 years ago. Evidence has mounted on the importance of parasite avoidance behaviours and it is increasingly apparent that there are core similarities in the function and benefit of this defence mechanism between terrestrial and aquatic systems. However, there are also stark differences driven by the unique biotic and abiotic characteristics of terrestrial and aquatic (marine and freshwater) environments. Here, we review avoidance behaviours in a comparative framework and highlight the characteristics of each environment that drive differences in the suite of mechanisms and cues that animals use to avoid parasites. We then explore trade-offs, potential negative effects of avoidance behaviour and the influence of human activities on avoidance behaviours. We conclude that avoidance behaviours are understudied in aquatic environments but can have significant implications for disease ecology and epidemiology, especially considering the accelerating emergence and re-emergence of parasites.peerReviewe