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.

Trophic relationship between the invasive parasitic copepod Mytilicola orientalis and its native blue mussel (Mytilus edulis) host.

Invasive parasites can spill over to new hosts in invaded ecosystems with often unpredictable trophic relationships in the newly arising parasite-host interactions. In European seas, the intestinal copepod Mytilicola orientalis was co-introduced with Pacific oysters (Magallana gigas) and spilled over to native blue mussels (Mytilus edulis), with negative impacts on the condition of infected mussels. However, whether the parasite feeds on host tissue and/or stomach contents is yet unknown. To answer this question, we performed a stable isotope analysis in which we included mussel host tissue and the primary food sources of the mussels, microphytobenthos (MPB) and particulate organic matter (POM). The copepods were slightly enriched in δ15N (mean Δ15N ± s.d.; 1·22 ± 0·58‰) and δ13C (Δ13C 0·25 ± 0·32‰) with respect to their host. Stable isotope mixing models using a range of trophic fractionation factors indicated that host tissue was the main food resource with consistent additional contributions of MPB and POM. These results suggest that the trophic relationship of the invasive copepod with its mussel host is parasitic as well as commensalistic. Stable isotope studies such as this one may be a useful tool to unravel trophic relationships in new parasite-host associations in the course of invasions.

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'.

Global invasion genetics of two parasitic copepods infecting marine bivalves.

Invasive species, and especially invasive parasites, represent excellent models to study ecological and evolutionary mechanisms in the wild. To understand these processes, it is crucial to obtain more knowledge on the native range, invasion routes and invasion history of invasive parasites. We investigated the consecutive invasions of two parasitic copepods (Mytilicola intestinalis and Mytilicola orientalis) by combining an extensive literature survey covering the reported putative native regions and the present-day invaded regions with a global phylogeography of both species. The population genetic analyses based on partial COI sequences revealed significant population differentiation for M. orientalis within the native region in Japan, while introduced populations in North America and Europe could not be distinguished from the native ones. Thus, M. orientalis' invasion history resembles the genetic structure and recent spread of its principal host, the Pacific oyster, Crassostrea gigas, while M. intestinalis lacks population genetic structure and has an overall low genetic diversity. Therefore, the native origin of M. intestinalis remains unclear. With this study, we demonstrate that even highly related and biologically similar invasive species can differ in their invasion genetics. From this, we conclude that extrapolating invasion genetics dynamics from related invasive taxa may not always be possible.

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.

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 Mytilicola intestinalis and its bivalve host, the blue mussel Mytilus edulis. 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.

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.