A global horizon scan of issues impacting marine and coastal biodiversity conservation.

The biodiversity of marine and coastal habitats is experiencing unprecedented change. While there are well-known drivers of these changes, such as overexploitation, climate change and pollution, there are also relatively unknown emerging issues that are poorly understood or recognized that have potentially positive or negative impacts on marine and coastal ecosystems. In this inaugural Marine and Coastal Horizon Scan, we brought together 30 scientists, policymakers and practitioners with transdisciplinary expertise in marine and coastal systems to identify new issues that are likely to have a significant impact on the functioning and conservation of marine and coastal biodiversity over the next 5-10 years. Based on a modified Delphi voting process, the final 15 issues presented were distilled from a list of 75 submitted by participants at the start of the process. These issues are grouped into three categories: ecosystem impacts, for example the impact of wildfires and the effect of poleward migration on equatorial biodiversity; resource exploitation, including an increase in the trade of fish swim bladders and increased exploitation of marine collagens; and new technologies, such as soft robotics and new biodegradable products. Our early identification of these issues and their potential impacts on marine and coastal biodiversity will support scientists, conservationists, resource managers and policymakers to address the challenges facing marine ecosystems.

Incorporating Biological Traits into Conservation Strategies.

Implementation of marine conservation strategies, such as increasing the numbers, extent, and effectiveness of protected areas (PAs), can help achieve conservation and restoration of ocean health and associated goods and services. Despite increasing recognition of the importance of including aspects of ecological functioning in PA design, the physical characteristics of habitats and simple measures of species diversity inform most PA designations. Marine and terrestrial ecologists have recently been using biological traits to assess community dynamics, functioning, and vulnerability to anthropogenic impacts. Here, we explore potential trait-based marine applications to advance PA design. We recommend strategies to integrate biological traits into (a) conservation objectives (e.g., by assessing and predicting impacts and vulnerability), (b) PA spatial planning (e.g., mapping ecosystem functions and functional diversity hot spots), and (c) time series monitoring protocols (e.g., using functional traits to detect recoveries). We conclude by emphasizing the need for pragmatic tools to improve the efficacy of spatial planning and monitoring efforts.

The BenBioDen database, a global database for meio-, macro- and megabenthic biomass and densities.

Benthic fauna refers to all fauna that live in or on the seafloor, which researchers typically divide into size classes meiobenthos (32/64 µm-0.5/1 mm), macrobenthos (250 µm-1 cm), and megabenthos (>1 cm). Benthic fauna play important roles in bioturbation activity, mineralization of organic matter, and in marine food webs. Evaluating their role in these ecosystem functions requires knowledge of their global distribution and biomass. We therefore established the BenBioDen database, the largest open-access database for marine benthic biomass and density data compiled so far. In total, it includes 11,792 georeferenced benthic biomass and 51,559 benthic density records from 384 and 600 studies, respectively. We selected all references following the procedure for systematic reviews and meta-analyses, and report biomass records as grams of wet mass, dry mass, or ash-free dry mass, or carbon per m2 and as abundance records as individuals per m2. This database provides a point of reference for future studies on the distribution and biomass of benthic fauna.

Climate change considerations are fundamental to management of deep-sea resource extraction.

Climate change manifestation in the ocean, through warming, oxygen loss, increasing acidification, and changing particulate organic carbon flux (one metric of altered food supply), is projected to affect most deep-ocean ecosystems concomitantly with increasing direct human disturbance. Climate drivers will alter deep-sea biodiversity and associated ecosystem services, and may interact with disturbance from resource extraction activities or even climate geoengineering. We suggest that to ensure the effective management of increasing use of the deep ocean (e.g., for bottom fishing, oil and gas extraction, and deep-seabed mining), environmental management and developing regulations must consider climate change. Strategic planning, impact assessment and monitoring, spatial management, application of the precautionary approach, and full-cost accounting of extraction activities should embrace climate consciousness. Coupled climate and biological modeling approaches applied in the water and on the seafloor can help accomplish this goal. For example, Earth-System Model projections of climate-change parameters at the seafloor reveal heterogeneity in projected climate hazard and time of emergence (beyond natural variability) in regions targeted for deep-seabed mining. Models that combine climate-induced changes in ocean circulation with particle tracking predict altered transport of early life stages (larvae) under climate change. Habitat suitability models can help assess the consequences of altered larval dispersal, predict climate refugia, and identify vulnerable regions for multiple species under climate change. Engaging the deep observing community can support the necessary data provisioning to mainstream climate into the development of environmental management plans. To illustrate this approach, we focus on deep-seabed mining and the International Seabed Authority, whose mandates include regulation of all mineral-related activities in international waters and protecting the marine environment from the harmful effects of mining. However, achieving deep-ocean sustainability under the UN Sustainable Development Goals will require integration of climate consideration across all policy sectors.

Resolving fine-scale population structure and fishery exploitation using sequenced microsatellites in a northern fish.

The resiliency of populations and species to environmental change is dependent on the maintenance of genetic diversity, and as such, quantifying diversity is central to combating ongoing widespread reductions in biodiversity. With the advent of next-generation sequencing, several methods now exist for resolving fine-scale population structure, but the comparative performance of these methods for genetic assignment has rarely been tested. Here, we evaluate the performance of sequenced microsatellites and a single nucleotide polymorphism (SNP) array to resolve fine-scale population structure in a critically important salmonid in north eastern Canada, Arctic Charr (Salvelinus alpinus). We also assess the utility of sequenced microsatellites for fisheries applications by quantifying the spatial scales of movement and exploitation through genetic assignment of fishery samples to rivers of origin and comparing these results with a 29-year tagging dataset. Self-assignment and simulation-based analyses of 111 genome-wide microsatellite loci and 500 informative SNPs from 28 populations of Arctic Charr in north-eastern Canada identified largely river-specific genetic structure. Despite large differences (~4X) in the number of loci surveyed between panels, mean self-assignment accuracy was similar with the microsatellite loci and the SNP panel (>90%). Subsequent analysis of 996 fishery-collected samples using the microsatellite panel revealed that larger rivers contribute greater numbers of individuals to the fishery and that coastal fisheries largely exploit individuals originating from nearby rivers, corroborating results from traditional tagging experiments. Our results demonstrate the efficacy of sequence-based microsatellite genotyping to advance understanding of fine-scale population structure and harvest composition in northern and understudied species.

Ecological variables for developing a global deep-ocean monitoring and conservation strategy.

The deep sea (>200 m depth) encompasses >95% of the world's ocean volume and represents the largest and least explored biome on Earth (<0.0001% of ocean surface), yet is increasingly under threat from multiple direct and indirect anthropogenic pressures. Our ability to preserve both benthic and pelagic deep-sea ecosystems depends upon effective ecosystem-based management strategies and monitoring based on widely agreed deep-sea ecological variables. Here, we identify a set of deep-sea essential ecological variables among five scientific areas of the deep ocean: (1) biodiversity; (2) ecosystem functions; (3) impacts and risk assessment; (4) climate change, adaptation and evolution; and (5) ecosystem conservation. Conducting an expert elicitation (1,155 deep-sea scientists consulted and 112 respondents), our analysis indicates a wide consensus amongst deep-sea experts that monitoring should prioritize large organisms (that is, macro- and megafauna) living in deep waters and in benthic habitats, whereas monitoring of ecosystem functioning should focus on trophic structure and biomass production. Habitat degradation and recovery rates are identified as crucial features for monitoring deep-sea ecosystem health, while global climate change will likely shift bathymetric distributions and cause local extinction in deep-sea species. Finally, deep-sea conservation efforts should focus primarily on vulnerable marine ecosystems and habitat-forming species. Deep-sea observation efforts that prioritize these variables will help to support the implementation of effective management strategies on a global scale.

Oceanographic variation influences spatial genomic structure in the sea scallop, Placopecten magellanicus.

Environmental factors can influence diversity and population structure in marine species and accurate understanding of this influence can both improve fisheries management and help predict responses to environmental change. We used 7163 SNPs derived from restriction site-associated DNA sequencing genotyped in 245 individuals of the economically important sea scallop, Placopecten magellanicus, to evaluate the correlations between oceanographic variation and a previously identified latitudinal genomic cline. Sea scallops span a broad latitudinal area (>10 degrees), and we hypothesized that climatic variation significantly drives clinal trends in allele frequency. Using a large environmental dataset, including temperature, salinity, chlorophyll a, and nutrient concentrations, we identified a suite of SNPs (285-621, depending on analysis and environmental dataset) potentially under selection through correlations with environmental variation. Principal components analysis of different outlier SNPs and environmental datasets revealed similar northern and southern clusters, with significant associations between the first axes of each (R2adj = .66-.79). Multivariate redundancy analysis of outlier SNPs and the environmental principal components indicated that environmental factors explained more than 32% of the variance. Similarly, multiple linear regressions and random-forest analysis identified winter average and minimum ocean temperatures as significant parameters in the link between genetic and environmental variation. This work indicates that oceanographic variation is associated with the observed genomic cline in this species and that seasonal periods of extreme cold may restrict gene flow along a latitudinal gradient in this marine benthic bivalve. Incorporating this finding into management may improve accuracy of management strategies and future predictions.

A climate-associated multispecies cryptic cline in the northwest Atlantic.

The spatial genetic structure of most species in the open marine environment remains largely unresolved. This information gap creates uncertainty in the sustainable management, recovery, and associated resilience of marine communities and our capacity to extrapolate beyond the few species for which such information exists. We document a previously unidentified multispecies biogeographic break aligned with a steep climatic gradient and driven by seasonal temperature minima in the northwest Atlantic. The coherence of this genetic break across our five study species with contrasting life histories suggests a pervasive macroecological phenomenon. The integration of this genetic structure with habitat suitability models and climate forecasts predicts significant variation in northward distributional shifts among populations and availability of suitable habitat in future oceans. The results of our integrated approach provide new perspective on how cryptic intraspecific diversity associated with climatic variation influences species and community response to climate change beyond simple poleward shifts.

Applying Movement Ecology to Marine Animals with Complex Life Cycles.

Marine animals with complex life cycles may move passively or actively for fertilization, dispersal, predator avoidance, resource acquisition, and migration, and over scales from micrometers to thousands of kilometers. This diversity has catalyzed idiosyncratic and unfocused research, creating unsound paradigms regarding the role of movement in ecology and evolution. The emerging movement ecology paradigm offers a framework to consolidate movement research independent of taxon, life-history stage, scale, or discipline. This review applies the framework to movement among life-history stages in marine animals with complex life cycles to consolidate marine movement research and offer insights for scientists working in aquatic and terrestrial realms. Irrespective of data collection or simulation strategy, breaking each life-history stage down into the fundamental units of movement allows each unit to be studied independently or interactively with other units. Understanding these underlying mechanisms of movement within each life-history stage can then be used to construct lifetime movement paths. These paths can allow further investigation of the relative contributions and interdependencies of steps and phases across a lifetime and how these paths influence larger research topics, such as population-level movements.

Global Carbon Cycling on a Heterogeneous Seafloor.

Diverse biological communities mediate the transformation, transport, and storage of elements fundamental to life on Earth, including carbon, nitrogen, and oxygen. However, global biogeochemical model outcomes can vary by orders of magnitude, compromising capacity to project realistic ecosystem responses to planetary changes, including ocean productivity and climate. Here, we compare global carbon turnover rates estimated using models grounded in biological versus geochemical theory and argue that the turnover estimates based on each perspective yield divergent outcomes. Importantly, empirical studies that include sedimentary biological activity vary less than those that ignore it. Improving the relevance of model projections and reducing uncertainty associated with the anticipated consequences of global change requires reconciliation of these perspectives, enabling better societal decisions on mitigation and adaptation.

The deep-sea under global change.

The deep ocean encompasses 95% of the oceans' volume and is the largest and least explored biome of Earth's Biosphere. New life forms are continuously being discovered. The physiological mechanisms allowing organisms to adapt to extreme conditions of the deep ocean (high pressures, from very low to very high temperatures, food shortage, lack of solar light) are still largely unknown. Some deep-sea species have very long life-spans, whereas others can tolerate toxic compounds at high concentrations; these characteristics offer an opportunity to explore the specialized biochemical and physiological mechanisms associated with these responses. Widespread symbiotic relationships play fundamental roles in driving host functions, nutrition, health, and evolution. Deep-sea organisms communicate and interact through sound emissions, chemical signals and bioluminescence. Several giants of the oceans hunt exclusively at depth, and new studies reveal a tight connection between processes in the shallow water and some deep-sea species. Limited biological knowledge of the deep-sea limits our capacity to predict future response of deep-sea organisms subject to increasing human pressure and changing global environmental conditions. Molecular tools, sensor-tagged animals, in situ and laboratory experiments, and new technologies can enable unprecedented advancement of deep-sea biology, and facilitate the sustainable management of deep ocean use under global change.

Identifying patterns of dispersal, connectivity and selection in the sea scallop, Placopecten magellanicus, using RADseq-derived SNPs.

Understanding patterns of dispersal and connectivity among marine populations can directly inform fisheries conservation and management. Advances in high-throughput sequencing offer new opportunities for estimating marine connectivity. We used restriction-site-associated DNA sequencing to examine dispersal and realized connectivity in the sea scallop Placopecten magellanicus, an economically important marine bivalve. Based on 245 individuals sampled rangewide at 12 locations from Newfoundland to the Mid-Atlantic Bight, we identified and genotyped 7163 single nucleotide polymorphisms; 112 (1.6%) were identified as outliers potentially under directional selection. Bayesian clustering revealed a discontinuity between northern and southern samples, and latitudinal clines in allele frequencies were observed in 42.9% of the outlier loci and in 24.6% of neutral loci. Dispersal estimates derived using these clines and estimates of linkage disequilibrium imply limited dispersal; 373.1 ± 407.0 km (mean ± SD) for outlier loci and 641.0 ± 544.6 km (mean ± SD) for neutral loci. Our analysis suggests restricted dispersal compared to the species range (>2000 km) and that dispersal and effective connectivity differ. These observations support the hypothesis that limited effective dispersal structures scallop populations along eastern North America. These findings can help refine the appropriate scale of management and conservation in this commercially valuable species.

An Ocean of Discovery: Biodiversity Beyond the Census of Marine Life.

The 70 % of Earth's surface covered by oceans supports significant biological diversity and immense untapped potential for marine bioproducts. The recently completed international Census of Marine Life (2000-2010) invested heavily in evaluating the diversity, abundance, and distribution of life in the ocean but concluded that at least 50 % and potentially > 90 % of marine species remain undescribed by science. Despite this potential, and numerous successes spanning pharmaceuticals, nutraceuticals, anti-foulants and adhesives, biofuels, biocatalysts (enzymes), and cosmetics, several impediments have slowed marine bioproduct development. First, the sheer size of the ocean constrains comprehensive exploration. Second, marine taxonomists and ecologists generally do not focus on the most promising groups for bioproduct development. Third, the geographic mismatch between (often remote) biodiversity hotspots and science capacity limit discovery. Despite these challenges, new ocean sampling tools (digital imaging, remote vehicles, genetic approaches, in situ samplers), many developed or improved during the Census of Marine Life, should enhance future marine biodiversity and thus marine bioproduct discovery.

Environmental Drivers of Benthic Flux Variation and Ecosystem Functioning in Salish Sea and Northeast Pacific Sediments.

The upwelling of deep waters from the oxygen minimum zone in the Northeast Pacific from the continental slope to the shelf and into the Salish Sea during spring and summer offers a unique opportunity to study ecosystem functioning in the form of benthic fluxes along natural gradients. Using the ROV ROPOS we collected sediment cores from 10 sites in May and July 2011, and September 2013 to perform shipboard incubations and flux measurements. Specifically, we measured benthic fluxes of oxygen and nutrients to evaluate potential environmental drivers of benthic flux variation and ecosystem functioning along natural gradients of temperature and bottom water dissolved oxygen concentrations. The range of temperature and dissolved oxygen encountered across our study sites allowed us to apply a suite of multivariate analyses rarely used in flux studies to identify bottom water temperature as the primary environmental driver of benthic flux variation and organic matter remineralization. Redundancy analysis revealed that bottom water characteristics (temperature and dissolved oxygen), quality of organic matter (chl a:phaeo and C:N ratios) and sediment characteristics (mean grain size and porosity) explained 51.5% of benthic flux variation. Multivariate analyses identified significant spatial and temporal variation in benthic fluxes, demonstrating key differences between the Northeast Pacific and Salish Sea. Moreover, Northeast Pacific slope fluxes were generally lower than shelf fluxes. Spatial and temporal variation in benthic fluxes in the Salish Sea were driven primarily by differences in temperature and quality of organic matter on the seafloor following phytoplankton blooms. These results demonstrate the utility of multivariate approaches in differentiating among potential drivers of seafloor ecosystem functioning, and indicate that current and future predictive models of organic matter remineralization and ecosystem functioning of soft-muddy shelf and slope seafloor habitats should consider bottom water temperature variation. Bottom temperature has important implications for estimates of seasonal and spatial benthic flux variation, benthic-pelagic coupling, and impacts of predicted ocean warming at high latitudes.

Long distance linkage disequilibrium and limited hybridization suggest cryptic speciation in atlantic cod.

Hybrid zones provide unprecedented opportunity for the study of the evolution of reproductive isolation, and the extent of hybridization across individuals and genomes can illuminate the degree of isolation. We examine patterns of interchromosomal linkage disequilibrium (ILD) and the presence of hybridization in Atlantic cod, Gadus morhua, in previously identified hybrid zones in the North Atlantic. Here, previously identified clinal loci were mapped to the cod genome with most (∼70%) occurring in or associated with (<5 kb) coding regions representing a diverse array of possible functions and pathways. Despite the observation that clinal loci were distributed across three linkage groups, elevated ILD was observed among all groups of clinal loci and strongest in comparisons involving a region of low recombination along linkage group 7. Evidence of ILD supports a hypothesis of divergence hitchhiking transitioning to genome hitchhiking consistent with reproductive isolation. This hypothesis is supported by Bayesian characterization of hybrid classes present and we find evidence of common F1 hybrids in several regions consistent with frequent interbreeding, yet little evidence of F2 or backcrossed individuals. This work suggests that significant barriers to hybridization and introgression exist among these co-occurring groups of cod either through strong selection against hybrid individuals, or genetic incompatibility and intrinsic barriers to hybridization. In either case, the presence of strong clinal trends, and little gene flow despite extensive hybridization supports a hypothesis of reproductive isolation and cryptic speciation in Atlantic cod. Further work is required to test the degree and nature of reproductive isolation in this species.

Challenging the paradigms of deep-sea ecology.

Deep-sea ecosystems represent Earth's major ecological research frontier. Focusing on seafloor ecosystems, we demonstrate how new technologies underpin discoveries that challenge major ecological hypotheses and paradigms, illuminating new deep-sea geosphere-biosphere interactions. We now recognize greater habitat complexity, new ecological interactions and the importance of 'dark energy', and chemosynthetic production in fuelling biodiversity. We also acknowledge functional hotspots that contradict a food-poor, metabolically inactive, and minor component of global carbon cycles. Symbioses appear widespread, revealing novel adaptations. Populations show complex spatial structure and evolutionary histories. These new findings redefine deep-sea ecology and the role of Earth's largest biome in global biosphere functioning. Indeed, deep-sea exploration can open new perspectives in ecological research to help mitigate exploitation impacts.

Real world biodiversity-ecosystem functioning: a seafloor perspective.

The effective application of biodiversity-ecosystem function (BEF) research to societal needs amid the Anthropocene represents the next grand challenge for ecology. Biodiversity knowledge that is most meaningful to society must reconcile insights derived from theory with detailed experiments and broad-scale trends. This perspective requires science that addresses high species richness, redundancy, and natural variability, which simplified 'model systems' cannot mimic. Here, we illustrate solutions of biodiversity knowledge to management and societal problems that combine BEF with scaling experiments, analysis of BEF along environmental gradients, and mapping technologies. We primarily draw examples from biophysical interactions in seafloor environments, which cover 70% of the Earth and add significantly to global ecosystem functions and services.