Multi-decadal trends in biomarkers in harp seal teeth from the North Atlantic reveal the influence of prey availability on seal trophic position.

Arctic food webs are being impacted by borealisation and environmental change. To quantify the impact of these multiple forcings, it is crucial to accurately determine the temporal change in key ecosystem metrics, such as trophic position of top predators. Here, we measured stable nitrogen isotopes (δ15 N) in amino acids in harp seal teeth from across the North Atlantic spanning a period of 60 years to robustly assess multi-decadal trends in harp seal trophic position, accounting for changes in δ15 N at the base of the food web. We reveal long-term variations in trophic position of harp seals which are likely to reflect fluctuations in prey availability, specifically fish- or invertebrate-dominated diets. We show that the temporal trends in harp seal trophic position differ between the Northwest Atlantic, Greenland Sea and Barents Sea, suggesting divergent changes in each local ecosystem. Our results provide invaluable data for population dynamic and ecotoxicology studies.

Multi-decadal environmental change in the Barents Sea recorded by seal teeth.

Multiple environmental forcings, such as warming and changes in ocean circulation and nutrient supply, are affecting the base of Arctic marine ecosystems, with cascading effects on the entire food web through bottom-up control. Stable nitrogen isotopes (δ15 N) can be used to detect and unravel the impact of these forcings on this unique ecosystem, if the many processes that affect the δ15 N values are constrained. Combining unique 60-year records from compound specific δ15 N biomarkers on harp seal teeth alongside state-of-the-art ocean modelling, we observed a significant decline in the δ15 N values at the base of the Barents Sea food web from 1951 to 2012. This strong and persistent decadal trend emerges due to the combination of anthropogenic atmospheric nitrogen deposition in the Atlantic, increased northward transport of Atlantic water through Arctic gateways and local feedbacks from increasing Arctic primary production. Our results suggest that the Arctic ecosystem has been responding to anthropogenically induced local and remote drivers, linked to changing ocean biology, chemistry and physics, for at least 60 years. Accounting for these trends in δ15 N values at the base of the food web is essential to accurately detect ecosystem restructuring in this rapidly changing environment.

Evidence of Vent-Adaptation in Sponges Living at the Periphery of Hydrothermal Vent Environments: Ecological and Evolutionary Implications.

The peripheral areas of deep-sea hydrothermal vents are often inhabited by an assemblage of animals distinct to those living close to vent chimneys. For many such taxa, it is considered that peak abundances in the vent periphery relate to the availability of hard substrate as well as the increased concentrations of organic matter generated at vents, compared to background areas. However, the peripheries of vents are less well-studied than the assemblages of vent-endemic taxa, and the mechanisms through which peripheral fauna may benefit from vent environments are generally unknown. Understanding this is crucial for evaluating the sphere of influence of hydrothermal vents and managing the impacts of future human activity within these environments, as well as offering insights into the processes of metazoan adaptation to vents. In this study, we explored the evolutionary histories, microbiomes and nutritional sources of two distantly-related sponge types living at the periphery of active hydrothermal vents in two different geological settings (Cladorhiza from the E2 vent site on the East Scotia Ridge, Southern Ocean, and Spinularia from the Endeavour vent site on the Juan de Fuca Ridge, North-East Pacific) to examine their relationship to nearby venting. Our results uncovered a close sister relationship between the majority of our E2 Cladorhiza specimens and the species Cladorhiza methanophila, known to harbor and obtain nutrition from methanotrophic symbionts at cold seeps. Our microbiome analyses demonstrated that both E2 Cladorhiza and Endeavour Spinularia sp. are associated with putative chemosynthetic Gammaproteobacteria, including Thioglobaceae (present in both sponge types) and Methylomonaceae (present in Spinularia sp.). These bacteria are closely related to chemoautotrophic symbionts of bathymodiolin mussels. Both vent-peripheral sponges demonstrate carbon and nitrogen isotopic signatures consistent with contributions to nutrition from chemosynthesis. This study expands the number of known associations between metazoans and potentially chemosynthetic Gammaproteobacteria, indicating that they can be incredibly widespread and also occur away from the immediate vicinity of chemosynthetic environments in the vent-periphery, where these sponges may be adapted to benefit from dispersed vent fluids.

Interactions between Environmental Contaminants and Gastrointestinal Parasites: Novel Insights from an Integrative Approach in a Marine Predator.

Environmental contaminants and parasites are ubiquitous stressors that can affect animal physiology and derive from similar dietary sources (co-exposure). To unravel their interactions in wildlife, it is thus essential to quantify their concurring drivers. Here, the relationship between blood contaminant residues (11 trace elements and 17 perfluoroalkyl substances) and nonlethally quantified gastrointestinal parasite loads was tested while accounting for intrinsic (sex, age, and mass) and extrinsic factors (trophic ecology inferred from stable isotope analyses and biologging) in European shags Phalacrocorax aristotelis. Shags had high mercury (range 0.65-3.21 µg g-1 wet weight, ww) and extremely high perfluorooctanoic acid (PFOA) and perfluorononanoic acid (PFNA) residues (3.46-53 and 4.48-44 ng g-1 ww, respectively). Males had higher concentrations of arsenic, mercury, PFOA, and PFNA than females, while the opposite was true for selenium, perfluorododecanoic acid (PFDoA), and perfluooctane sulfonic acid (PFOS). Individual parasite loads (Contracaecum rudolphii) were higher in males than in females. Females targeted pelagic-feeding prey, while males relied on both pelagic- and benthic-feeding organisms. Parasite loads were not related to trophic ecology in either sex, suggesting no substantial dietary co-exposure with contaminants. In females, parasite loads increased strongly with decreasing selenium:mercury molar ratios. Females may be more susceptible to the interactive effects of contaminants and parasites on physiology, with potential fitness consequences.

Pelagic vs Coastal-Key Drivers of Pollutant Levels in Barents Sea Polar Bears with Contrasted Space-Use Strategies.

In the Barents Sea, pelagic and coastal polar bears are facing various ecological challenges that may explain the difference in their pollutant levels. We measured polychlorinated biphenyls, organochlorine pesticides, polybrominated diphenyl ethers in fat, and perfluoroalkyl substances in plasma in pelagic and coastal adult female polar bears with similar body condition. We studied polar bear feeding habits with bulk stable isotope ratios of carbon and nitrogen. Nitrogen isotopes of amino acids were used to investigate their trophic position. We studied energy expenditure by estimating field metabolic rate using telemetry data. Annual home range size was determined, and spatial gradients in pollutants were explored using latitude and longitude centroid positions of polar bears. Pollutant levels were measured in harp seals from the Greenland Sea and White Sea-Barents Sea as a proxy for a West-East gradient of pollutants in polar bear prey. We showed that pelagic bears had higher pollutant loads than coastal bears because (1) they feed on a higher proportion of marine and higher trophic level prey, (2) they have higher energy requirements and higher prey consumption, (3) they forage in the marginal ice zones, and (4) they feed on prey located closer to pollutant emission sources/transport pathways.

Temporal and spatial trends in marine carbon isotopes in the Arctic Ocean and implications for food web studies.

The Arctic is undergoing unprecedented environmental change. Rapid warming, decline in sea ice extent, increase in riverine input, ocean acidification and changes in primary productivity are creating a crucible for multiple concurrent environmental stressors, with unknown consequences for the entire arctic ecosystem. Here, we synthesized 30 years of data on the stable carbon isotope (δ13 C) signatures in dissolved inorganic carbon (δ13 C-DIC; 1977-2014), marine and riverine particulate organic carbon (δ13 C-POC; 1986-2013) and tissues of marine mammals in the Arctic. δ13 C values in consumers can change as a result of environmentally driven variation in the δ13 C values at the base of the food web or alteration in the trophic structure, thus providing a method to assess the sensitivity of food webs to environmental change. Our synthesis reveals a spatially heterogeneous and temporally evolving δ13 C baseline, with spatial gradients in the δ13 C-POC values between arctic shelves and arctic basins likely driven by differences in productivity and riverine and coastal influence. We report a decline in δ13 C-DIC values (-0.011‰ per year) in the Arctic, reflecting increasing anthropogenic carbon dioxide (CO2 ) in the Arctic Ocean (i.e. Suess effect), which is larger than predicted. The larger decline in δ13 C-POC values and δ13 C in arctic marine mammals reflects the anthropogenic CO2 signal as well as the influence of a changing arctic environment. Combining the influence of changing sea ice conditions and isotopic fractionation by phytoplankton, we explain the decadal decline in δ13 C-POC values in the Arctic Ocean and partially explain the δ13 C values in marine mammals with consideration of time-varying integration of δ13 C values. The response of the arctic ecosystem to ongoing environmental change is stronger than we would predict theoretically, which has tremendous implications for the study of food webs in the rapidly changing Arctic Ocean.

Megafaunal variation in the abyssal landscape of the Clarion Clipperton Zone.

The potential for imminent polymetallic nodule mining in the Clarion Clipperton Fracture Zone (CCZ) has attracted considerable scientific and public attention. This concern stems from both the extremely large seafloor areas that may be impacted by mining, and the very limited knowledge of the fauna and ecology of this region. The environmental factors regulating seafloor ecology are still very poorly understood. In this study, we focus on megafaunal ecology in the proposed conservation zone 'Area of Particular Environmental Interest 6' (study area centred 17°16'N, 122°55'W). We employ bathymetric data to objectively define three landscape types in the area (a level bottom Flat, an elevated Ridge, a depressed Trough; water depth 3950-4250 m) that are characteristic of the wider CCZ. We use direct seabed sampling to characterise the sedimentary environment in each landscape, detecting no statistically significant differences in particle size distributions or organic matter content. Additional seafloor characteristics and data on both the metazoan and xenophyophore components of the megafauna were derived by extensive photographic survey from an autonomous underwater vehicle. Image data revealed that there were statistically significant differences in seafloor cover by nodules and in the occurrence of other hard substrata habitat between landscapes. Statistically significant differences in megafauna standing stock, functional structuring, diversity, and faunal composition were detected between landscapes. The Flat and Ridge areas exhibited a significantly higher standing stock and a distinct assemblage composition compared to the Trough. Geomorphological variations, presumably regulating local bottom water flows and the occurrence of nodule and xenophyophore test substrata, between study areas may be the mechanism driving these assemblage differences. We also used these data to assess the influence of sampling unit size on the estimation of ecological parameters. We discuss these results in the contexts of regional benthic ecology and the appropriate management of potential mining activities in the CCZ and elsewhere in the deep ocean.

Feeding preferences of abyssal macrofauna inferred from in situ pulse chase experiments.

Climatic fluctuations may significantly alter the taxonomic and biochemical composition of phytoplankton blooms and subsequently phytodetritus, the food source for the majority of deep-sea communities. To examine the response of abyssal benthic communities to different food resources we simulated a food sedimentation event containing diatoms and coccolithophorids at Station M in the NE Pacific. In one set of experiments we measured incorporation of diatomC and coccoN into the macrofauna using isotopically enriched (13)C-diatoms and (15)N-coccolithophores. In a second experiment we measured incorporation of C and N from dual-labelled ((13)C and (15)N) diatoms. The second experiment was repeated 2 months later to assess the effect of seasonality. The simulated food pulses represented additions of 650 - 800 mg C m(-2) and 120 mg N m(-2) to the seafloor. In all cases rapid incorporation of tracer was observed within 4 days, with between 20% and 52% of the macrofauna displaying evidence of enrichment. However, incorporation levels of both diatomC and coccoN were low (<0.05% and 0.005% of the added C and N). Incorporation of labelled diatoms was similar during both June and September suggesting that the community was not food limited during either period. We found no evidence for selective ingestion of the different food types in the metazoan fauna suggesting that macrofauna do not have strong preferences for diatom vs. coccolithophore dominated phytodetrital pulses. C∶N ratios from both experiments suggest that the metazoan macrofauna community appear to have higher C demands and/or assimilation efficiencies compared to N. Concomitantly, the foraminifera preferentially selected for diatomN over coccoN, and we suggest that this may be related to foraminiferal requirements for intracellular nitrate. These experiments provide evidence that abyssal faunal feeding strategies are in part driven by an organism's internal stoichiometric budgets and biochemical requirements.