Body condition and energy content of the shore crab Carcinus maenas L. in a temperate coastal system: the cost of barnacle epibiosis.

The impact of barnacle epibionts on the condition of the shore crab Carcinus maenas was studied for the western Wadden Sea population. Approximately 39% of the crabs were fouled with the barnacle Balanus crenatus. Although the morphological Fulton's K condition decreased by 5.8% in fouled crabs, Linear Mixed-Effects Models (LMM) showed that only the energetic condition of the crabs was significantly affected by fouling. The energy density of fouled crabs was consistently poorer (4.1% in AFDW; 8.7% in dry weight) than that of non-fouled crabs, especially in females and green forms in dry weight (12.8% and 11.4% reduction, respectively). Cumulative infection with Sacculina carcini, detected in 4.5% of the fouled crabs, additionally reduced by 14.3% the energy density in dry weight and almost to half of the total energy of the fouled crabs. Impacts of energy density reduction on crabs' growth and reproduction are discussed.

Sacculina carcini impact on energy content of the shore crab Carcinus maenas L.

The impact of Sacculina carcini infection on the nutritional status of the shore crab Carcinus maenas was investigated in the western Dutch Wadden Sea for a period of 20 months. About 3.3% of the population was sacculinized, i.e. externally infected with S. carcini and only 0.7% presented scars of previous infection. The results of mixed linear models showed that sacculinized and non-sacculinized crabs had similar morphometric condition, while the energy density of parasitized crabs (externa excluded) was significantly reduced by about 4.3% overall, and by up to 5.8% in crabs under 40 mm carapace width. However, when Sacculina externa was included in the energy determinations, the difference in energy density decreased to 1.2%, while total energy content of the pair infected crab-parasite including externa was 30.8% higher than non-sacculinized crabs of similar size. The total energy content of ovigerous females (eggs included) was even higher, near doubling the energy of similar-sized crabs. The same way, total energy content of Sacculina externa was about 4 times lower than total energy of egg mass. The results suggest that the rhizocephalan parasite is efficient in consuming the energy that the host may allocate for growth and maintenance, but require future studies to disentangle the impact of the degree of internal infection and the implications for the dynamics of the population.

Quantification of marine benthic communities with metabarcoding.

DNA metabarcoding methods have been implemented in studies aimed at detecting and quantifying marine benthic biodiversity. In such surveys, universal barcodes are amplified and sequenced from environmental DNA. To quantify biodiversity with DNA metabarcoding, a relation between the number of DNA sequences of a species and its biomass and/or the abundance is required. However, this relationship is complicated by many factors, and it is often unknown. In this study, we validate estimates of biomass and abundance from molecular approaches with those from the traditional morphological approach. Abundance and biomass were quantified from 126 samples of benthic intertidal mudflat using traditional morphological approaches and compared with frequency of occurrence and relative read abundance estimates from a molecular approach. A relationship between biomass and relative read abundance was found for two widely dispersed annelid taxa (Pygospio and Scoloplos). None of the other taxons, however, showed such a relationship. We discuss how quantification of abundance and biomass using molecular approaches are hampered by the ecology of DNA i.e. all the processes that determine the amount of DNA in the environment, including the ecology of the benthic species as well as the compositional nature of sequencing data.

No evidence for reduced growth in resident fish species in the era of de-eutrophication in a coastal area in NW Europe.

Coastal areas in north-western Europe have been influenced by elevated nutrient levels starting in the 1960s. Due to efficient measures, both nitrate and phosphate levels decreased since the mid-1980s. The co-occurring declines in nutrient loadings and fish productivity are often presumed to be causally linked. We investigated whether four resident fish species (twaite shad, bull-rout, thick-lipped grey mullet and eelpout), that spend the majority of their life in the vicinity of the coast, differed in growth between the historic eutrophication period compared to the recent lower nutrient-level period. Based on Von Bertalanffy growth models of length at age, and the analysis of annual otolith increments, we investigated the difference in sex-specific growth patterns and related these to temperature, eutrophication level (Chlorophyll a), growth window and fish density. In all four species, annual otolith growth rates during the early life stages differed between the two periods, mostly resulting in larger lengths at age in the recent period. All species showed significant correlations between increment size and temperature, explaining the observed period differences. The lack of an effect of total fish biomass provided no evidence for density dependent growth. A correlation with chlorophyll was found in bull-rout, but the relationship was negative, thus not supporting the idea of growth enhanced by high nutrient levels. In conclusion, we found no evidence for reduced growth related to de-eutrophication. Our results indicate that temperature rise due to climate change had a greater impact on growth than reduced food availability due to de-eutrophication. We discuss potential consequences of growth changes for length-based indicators used in management.

Here are the polyps: in situ observations of jellyfish polyps and podocysts on bivalve shells.

Most Scyphozoan jellyfish species have a metagenic life cycle involving a benthic, asexually reproducing polyp stage and a sexually reproducing medusa stage. Medusae can be large and conspicuous and most can be identified using morphological characteristics. Polyps on the other hand are small, live a cryptic life attached to hard substrates and often are difficult or impossible to distinguish based on morphology alone. Consequently, for many species the polyp stage has not been identified in the natural environment. We inspected hard substrates in various habitats for the presence of Scyphozoan polyps. Three polyps were found on Dogger Bank, Central North Sea, attached to the inside of the umbo of empty valves of the bivalves Mactra stultorum and Spisula subtruncata. One polyp was accompanied by four podocysts. With this knowledge, the inside of bivalve shells washed ashore in Oostende (Belgium) was inspected and supposed podocysts on the inside of empty valves of Cerastoderma edule and Spisula elliptica were found. Polyps and podocysts were identified to species level by 18S rDNA and mitochondrial COI sequencing. The three polyps found on Dogger Bank all belonged to the compass jellyfish Chrysaora hysoscella. One podocyst from the Oostende beach also belonged to this species but another podocyst belonged to Cyanea lamarkii. These are the first in situ observations of C. hysoscella and C. lamarckii polyps and podocysts in the natural environment. Mactra, Cerastoderma and Spisula species are abundant in many North Sea regions and empty bivalve shells could provide an abundant settling substrate for jellyfish polyps in the North Sea and other areas. Several new strategies to increase the detection of polyps on bivalve shells are presented.

Seasonal variation in the diet of estuarine bivalves.

Estuarine food webs are generally considered to be supported by marine pelagic and benthic primary producers and by the import of dead organic matter from the open sea. Although estuaries receive considerable amounts of freshwater phytoplankton and organic compounds from adjacent rivers, the potential contribution of these living and dead matter to estuarine food webs is often assumed to be negligible and, therefore, not examined. Based on stable isotope analyses, we report the importance of freshwater suspended particulate organic matter (FW-SPOM) for fuelling estuarine food webs in comparison to estuarine SPOM and microphytobenthos. This previously neglected food source contributed 50-60% (annual average) of food intake of suspension-feeding bivalves such as cockles (Cerastoderma edule), mussels (Mytilus edulis) and Pacific oysters (Magallana gigas) at the Balgzand tidal flats, an estuarine site in the western Wadden Sea (12-32 psu). For these species, this proportion was particularly high in autumn during strong run-off of SPOM-rich freshwater, whilst estuarine SPOM (20%-25%) and microphytobenthos (15%-30%) were relatively important in summer when the freshwater run-off was very low. These findings have implications for our understanding of the trophic interactions within coastal food webs and for freshwater management of estuarine ecosystems.

Presence-absence of marine macrozoobenthos does not generally predict abundance and biomass.

Many monitoring programmes of species abundance and biomass increasingly face financial pressures. Occupancy is often easier and cheaper to measure than abundance or biomass. We, therefore, explored whether measuring occupancy is a viable alternative to measuring abundance and biomass. Abundance- or biomass-occupancy relationships were studied for sixteen macrozoobenthos species collected across the entire Dutch Wadden Sea in eight consecutive summers. Because the form and strength of these relationships are scale-dependent, the analysis was completed at different spatiotemporal scales. Large differences in intercept and slope of abundance- or biomass-occupancy relationships were found. Abundance, not biomass, was generally positively correlated with occupancy. Only at the largest scale, seven species showed reasonably strong abundance-occupancy relationships with large coefficients of determination and small differences in observed and predicted values (RMSE). Otherwise, and at all the other scales, intraspecific abundance and biomass relationships were poor. Our results showed that there is no generic relationship between a species' abundance or biomass and its occupancy. We discuss how ecological differences between species could cause such large variation in these relationships. Future technologies might allow estimating a species' abundance or biomass directly from eDNA sampling data, but for now, we need to rely on traditional sampling technology.

Unexpected dietary preferences of Eurasian Spoonbills in the Dutch Wadden Sea: spoonbills mainly feed on small fish not shrimp.

After an historical absence, over the last decades Eurasian Spoonbills Platalea leucorodia leucorodia have returned to breed on the barrier islands of the Wadden Sea. The area offers an abundance of predator-free nesting habitat, low degrees of disturbance, and an extensive intertidal feeding area with increasing stocks of brown shrimp Crangon crangon, the assumed main prey of P. leucorodia leucorodia. Nevertheless, newly established and expanding colonies of spoonbills have surprisingly quickly reached plateau levels. Here we tested the often stated assertion that spoonbills mainly rely on brown shrimp as food, by quantifying the diet of chicks on the basis of regurgitates and by analysis of blood isotopes using stable isotope Bayesian mixing models. Both methods showed that, rather than brown shrimp being the staple food of spoonbill chicks, small flatfish (especially plaice Pleuronectes platessa) and gobies (Pomatoschistus spp.) were their main prey. Unlike shrimp, small flatfish have been reported to be rather scarce in the Wadden Sea in recent years, which may explain the rapid saturation of colony size due to food-related density-dependent recruitment declines of growing colonies. By way of their diet and colony growth characteristics, spoonbills may thus indicate the availability of small fish in the Wadden Sea. We predict that the recovery to former densities of young flatfish and other juvenile/small fish in the Wadden Sea will be tracked by changing diets (more fish) and an increase in the size of Eurasian Spoonbill colonies across the Wadden Sea.

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.

Where are the polyps? Molecular identification, distribution and population differentiation of Aurelia aurita jellyfish polyps in the southern North Sea area.

For many species of metagenic jellyfish the location of the benthic polyps is unknown. To gain insight in the distribution, species composition and population structure of scyphozoan jellyfish polyps in the southern North Sea area, polyp samples were collected from natural and artificial substrates (settling plates, marina floats and wrecks) at ten inshore locations in the Netherlands, seven offshore locations in the North Sea and in the Gullmar Fjord in Sweden. Polyps were identified to species level by sequencing both a fragment of 18S rDNA and a fragment of mitochondrial COI, and comparing these sequences to reference sequences available in GenBank and to newly obtained sequences from medusae collected in the area. All polyps sequenced did belong to Aurelia aurita. For this species, molecular diversity in mitochondrial COI was high, with 50 haplotypes among 183 polyps. Population differentiation was detected between the Dogger Bank and other-more coastal-locations, indicating extremely low connectivity. No significant differences were found between coastal samples. The location of polyps of Cyanea capillata, Cyanea lamarckii, Chrysaora hysoscella and Rhizostoma octopus in the study area remains unresolved.

How habitat-modifying organisms structure the food web of two coastal ecosystems.

The diversity and structure of ecosystems has been found to depend both on trophic interactions in food webs and on other species interactions such as habitat modification and mutualism that form non-trophic interaction networks. However, quantification of the dependencies between these two main interaction networks has remained elusive. In this study, we assessed how habitat-modifying organisms affect basic food web properties by conducting in-depth empirical investigations of two ecosystems: North American temperate fringing marshes and West African tropical seagrass meadows. Results reveal that habitat-modifying species, through non-trophic facilitation rather than their trophic role, enhance species richness across multiple trophic levels, increase the number of interactions per species (link density), but decrease the realized fraction of all possible links within the food web (connectance). Compared to the trophic role of the most highly connected species, we found this non-trophic effects to be more important for species richness and of more or similar importance for link density and connectance. Our findings demonstrate that food webs can be fundamentally shaped by interactions outside the trophic network, yet intrinsic to the species participating in it. Better integration of non-trophic interactions in food web analyses may therefore strongly contribute to their explanatory and predictive capacity.

Early contamination of European flounder (Platichthys flesus) by PCDD/Fs and dioxin-like PCBs in European waters.

Contamination levels and profiles of 7 polychlorinated-p-dioxins, 10 polychlorinated furans (PCDD/Fs) and 12 dioxin-like polychlorinated biphenyls (dl-PCBs) were investigated in juvenile European flounder (Platichthys flesus) captured in different nursery areas in the northeastern Atlantic coast across its geographical distribution range. The toxic equivalent concentrations (WHO-TEQfish) were also determined in order to evaluate which P. flesus population was more exposed to dioxin-like toxicity. Juveniles caught in the Sørfjord (Norway) showed the lowest WHO-TEQfish concentration (0.052 pg WHO-TEQfish g(-1)wet weight) whereas the highest value was observed in fish from the Wadden Sea (The Netherlands; 0.291 pg WHO-TEQfish g(-1)ww), mainly due to the greater contribution of 2,3,7,8-tetrachlorodibenzo-p-dioxin, the most toxic congener. Nonetheless, when comparing the results with existent tissue residue-based toxicity benchmarks, no adverse effects resulting from PCDD/Fs and dl-PCBs are expected to occur in flounder from the studied systems.

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts.

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.

Temperature tolerance and energetics: a dynamic energy budget-based comparison of North Atlantic marine species.

Temperature tolerance and sensitivity were examined for some North Atlantic marine species and linked to their energetics in terms of species-specific parameters described by dynamic energy budget (DEB) theory. There was a general lack of basic information on temperature tolerance and sensitivity for many species. Available data indicated that the ranges in tolerable temperatures were positively related to optimal growth temperatures. However, no clear relationships with temperature sensitivity were established and no clear differences between pelagic and demersal species were observed. The analysis was complicated by the fact that for pelagic species, experimental data were completely absent and even for well-studied species, information was incomplete and sometimes contradictory. Nevertheless, differences in life-history strategies were clearly reflected in parameter differences between related species. Two approaches were used in the estimation of DEB parameters: one based on the assumption that reserve hardly contributes to physical volume; the other does not make this assumption, but relies on body-size scaling relationships, using parameter values of a generalized animal as pseudo-data. Temperature tolerance and sensitivity seemed to be linked with the energetics of a species. In terms of growth, relatively high temperature optima, sensitivity and/or tolerance were related to lower relative assimilation rates as well as lower maintenance costs. Making the step from limited observations to underlying mechanisms is complicated and extrapolations should be carefully interpreted. Special attention should be devoted to the estimation of parameters using body-size scaling relationships predicted by the DEB theory.

Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range.

The common or brown shrimp Crangon crangon (L.) is a highly abundant and important taxon, both ecologically and commercially, yet knowledge on its population structure and historical biogeography is limited. We studied population genetic structure across the distribution range of this species by sequencing a 388 bp fragment of the cytochrome-c-oxidase I gene for 140 individuals from 25 locations. Strong population structuring and high levels of genetic diversity were observed. Four main phylogroups were uncovered: northeastern Atlantic, western Mediterranean, Adriatic Sea and Black Sea. Gene flow of these shrimp across known oceanographical barriers (e.g., the Strait of Gibraltar and/or Oran-Almeria front, Sicilian Straits, and Turkish Straits) is severely restricted. The oldest and most variable populations currently inhabit the western Mediterranean. The observed absence of structure across the entire northeastern Atlantic shelf is proposed not to be due to gene flow, but to relatively recent colonization following the glacial cycles of the late Pleistocene. Black Sea shrimp are currently disconnected from Mediterranean populations, and colonization is inferred, on the basis of coalescent analysis, to have happened relatively recently, but possibly earlier than 7000 years ago. We postulate the hypothesis that C. crangon survived the last brackish-water (<7 per thousand) period inside the Black Sea and/or one of the adjacent inland seas. We conclude that (1) common shrimp populations from different basins are strongly differentiated, (2) gene flow across basins is probably very limited, and (3) the biogeographic history of the taxon is largely in accordance with the geographic history of its distribution range. This study provides further evidence that high population connectivity of marine species (e.g., by policy makers) should not be assumed.

Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.).

Overexploitation and subsequent collapses of major worldwide fisheries has made it clear that marine stocks are no inexhaustible. Unfortunately, the perception remains that marine fished are resilient to large population reductions, as even a commercially 'collapsed' stock will still consist of millions of individuals. Coupled with this notion is the idea that fisheries can, therefore, have little effect on the genetic diversity of stocks. We used DNA from archived otoliths collected between 1924 and 1972 together with 2002 juvenile;s tissue to estimate effective population size (Ne) in plaice (Pleuronrctes platessa). Ne was estimated at 20,000 in the North Sea and 2000 in Iceland. These values are five orders of magnitude smaller than the estimated census size foe the two locations. Populations examined between 1924 and 1960 were in Hardy-Weinberg equilibrium, whereas populations examined after 1970 were not. Extensive testing was performed to rule out genotyping artefacts and Wahlund effects. The significant heterozygote deficiencies found from 1970 onward were attributed to inbreeding. The emergence of inbreeding between 1905 and 19070 coincides with the increase in fishing mortality after World War II. Although the biological mechanisms remain speculative, our demonstration of inbreeding signals the need for understanding the social and mating behaviour in commercially important fishes.