M. Anouk Goedknegt

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 organisms 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.

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.

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.

Impact of the invasive parasitic copepod Mytilicola orientalis on native blue mussels Mytilus edulis in the western European Wadden Sea

ABSTRACT Invasive species can indirectly affect native species by modifying parasite–host dynamics and disease occurrence. This scenario applies to European coastal waters where the invasive Pacific oyster (Magallana gigas) co-introduced the parasitic copepod Mytilicola orientalis that spills over to native blue mussels (Mytilus edulis) and other native bivalves. In this study, we investigated the impact of M. orientalis infections on blue mussels by conducting laboratory experiments using controlled infections with larval stages of the parasitic copepod. As the impact of infections is likely to depend on the mussels’ food availability, we also tested whether potential adverse effects of infection on mussels intensify under low food conditions. Blue mussels that were experimentally infected with juvenile M. orientalis had a significantly lower body condition (11–13%) compared with uninfected mussels after nine weeks of infection. However, naturally infected mussels from a mixed mussel and oyster bed did not significantly differ in body condition compared with uninfected mussels. Contrary to effects on mussel condition, we did not find an effect of experimental infections on clearance rates, shell growth or survival of blue mussels and no clear sign of exacerbating effects of food limitation. Our study illustrates that invasive species can indirectly affect native species via parasite co-introductions and parasite spillover. The results of this study call for the integration of such parasite-mediated indirect effects of invasions in impact assessments of invasive species.