Deeply hidden inside introduced biogenic structures – Pacific oyster reefs reduce detrimental barnacle overgrowth on native blue mussels

In sedimentary coastal ecosystems shells of epibenthic organisms such as blue mussels (Mytilus edulis) provide the only major attachment surface for barnacle epibionts, which may cause detrimental effects on their mussel basibionts by e.g. reducing growth rate. In the European Wadden Sea, beds of native blue mussels have been invaded by Pacific oysters Crassostrea gigas, which transformed these beds into mixed reefs of oysters with mussels. In this study, we determined the spatial distribution of M. edulis and their barnacle epibionts (Semibalanus balanoides) within the reef matrix. Mean mussel density near the bottom was about twice as high compared to the mussel density near the top of an oyster reef, whereas barnacles on mussels showed a reversed pattern. Barnacle dry weight per mussel was on average 14 times higher near the top than at the bottom. This patternwas confirmed by experimentally placing clean M. edulis at the top and on the bottomof oyster reefs at two sites in the Wadden Sea (island of Texel, The Netherlands; island of Sylt, Germany). After an experimental period of fiveweeks (April and May 2015, the main settlement period of S. balanoides), the number of barnacles per mussel was at both sites significantly higher on mussels near the top compared to near the bottom. We conclude that the oyster reef matrix offers a refuge for M. edulis: inside reefs they are not only better protected against predators but also against detrimental barnacle overgrowth. This study shows that alien species can cause beneficial effects for native organisms and should not be generally considered as a risk for the recipientmarine ecosystems

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

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

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

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

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

How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale

There are surprisingly few field studies on the role of invasive species on parasite infection patterns in native hosts. We investigated the role of invasive Pacific oysters (Magallana gigas) in determining parasite infection levels in native blue mussels (Mytilus edulis) in relation to other environmental and biotic factors. Using hierarchical field sampling covering three spatial scales along a large intertidal ecosystem (European Wadden Sea), we found strong spatial differences in infection levels of five parasite species associated with mussels and oysters. We applied mixed models to analyse the associations between parasite prevalence and abundance in mussels and oysters, and 12 biological and environmental factors. For each parasite–host relationship, an optimal model (either a null, one-factor or two-factor model) was selected based on AIC scores. We found that the density of invasive oysters contributed to three of the 12 models. Other biological factors such as host size (six models), and the density of target or alternative host species (five models) contributed more frequently to the best models. Furthermore, for parasite species infecting both mussels and oysters, parasite population densities were higher in native mussels, attributed to the higher densities of mussels. Our results indicate that invasive species can affect parasite infection patterns in native species in the field, but that their relative contribution may be further mediated by other biological and environmental parameters. These results stress the usefulness of large-scale field studies for detailed assessments of the mechanisms underlying the impacts of invasive species on native host communities

Ecosystem services provided by a non-cultured shellfish species: the common cockle Cerastoderma edule

Coastal habitats provide many important ecosystem services. The substantial role of shellfish in delivering ecosystem services is increasingly recognised, usually with a focus on cultured species, but wild-harvested bivalve species have largely been ignored. This study aimed to collate evidence and data to demonstrate the substantial role played by Europe's main wild-harvested bivalve species, the common cockle Cerastoderma edule, and to assess the ecosystem services that cockles provide. Data and information are synthesised from five countries along the Atlantic European coast with a long history of cockle fisheries. The cockle helps to modify habitat and support biodiversity, and plays a key role in the supporting services on which many of the other services depend. As well as providing food for people, cockles remove nitrogen, phosphorus and carbon from the marine environment, and have a strong cultural influence in these countries along the Atlantic coast. Preliminary economic valuation of some of these services in a European context is provided, and key knowledge gaps identified. It is concluded that the cockle has the potential to become (i) an important focus of conservation and improved sustainable management practices in coastal areas and communities, and (ii) a suitable model species to study the integration of cultural ecosystem services within the broader application of ‘ecosystem services’

Inter‐country differences in the cultural ecosystem services provided by cockles

1. Coastal systems provide many cultural ecosystem services (CES) to humans. Fewer studies have focused solely on CES, while those comparing CES across countries are even rarer. In the case of shellfish, considerable ecosystem services focus has been placed on nutrient remediation, with relatively little on the cultural services provided, despite strong historical, cultural, social and economic links between shellfish and coastal communities. The ecosystem services provided by the common cockle, Cerastoderma edule, have recently been described, yet the cultural benefits from cockles remain mostly unknown. 2. Here, we documented the CES provided by C. edule in five maritime countries along the Atlantic coast of western Europe, classifying evidenced examples of services into an a priori framework. The high-level classes, adapted from the Millennium Assessment and the Common International Classification of Ecosystem Services, were: inspirational, sense of place, spiritual & religious, aesthetic, recreation & ecotourism, cultural heritage and educational. A further 19 sub-classes were defined. We followed a narrative approach to draw out commonalities and differences among countries using a semi-quantitative analysis. 3. Examples of CES provided by cockles were found for all classes in most countries. Cockles supply important and diverse cultural benefits to humans across Atlantic Europe, making it an ideal model species to study CES in coastal areas. Most examples were in cultural heritage, highlighting the importance of this class in comparison with classes which typically receive more attention in the literature like recreation or aesthetics. We also found that the cultural associations with cockles differed among countries, including between neighbouring countries that share a strong maritime heritage. The extent to which cultural associations were linked with the present or past also differed among countries, with stronger association with the present in southern countries and with the past in the north. 4. Understanding the wider benefits of cockles could deepen the recognition of this important coastal resource, and contribute to promoting sustainable management practices, through greater engagement with local communities. This study is an important step towards better integration of CES in coastal environments and could be used as a framework to study the CES of other species or ecosystems