Discovering marine biodiversity in the 21st century.

We review the current knowledge of the biodiversity of the ocean as well as the levels of decline and threat for species and habitats. The lack of understanding of the distribution of life in the ocean is identified as a significant barrier to restoring its biodiversity and health. We explore why the science of taxonomy has failed to deliver knowledge of what species are present in the ocean, how they are distributed and how they are responding to global and regional to local anthropogenic pressures. This failure prevents nations from meeting their international commitments to conserve marine biodiversity with the results that investment in taxonomy has declined in many countries. We explore a range of new technologies and approaches for discovery of marine species and their detection and monitoring. These include: imaging methods, molecular approaches, active and passive acoustics, the use of interconnected databases and citizen science. Whilst no one method is suitable for discovering or detecting all groups of organisms many are complementary and have been combined to give a more complete picture of biodiversity in marine ecosystems. We conclude that integrated approaches represent the best way forwards for accelerating species discovery, description and biodiversity assessment. Examples of integrated taxonomic approaches are identified from terrestrial ecosystems. Such integrated taxonomic approaches require the adoption of cybertaxonomy approaches and will be boosted by new autonomous sampling platforms and development of machine-speed exchange of digital information between databases.

Habitat Protection Indexes - new monitoring measures for the conservation of coastal and marine habitats.

A worldwide call to implement habitat protection aims to halt biodiversity loss. We constructed an open-source, standardized, and reproducible workflow that calculates two indexes to monitor the extent of coastal and marine habitats within protected areas and other effective area-based conservation measures. The Local Proportion of Habitats Protected Index (LPHPI) pinpoints the jurisdictions with the greatest opportunity to expand their protected or conserved areas, while the Global Proportion of Habitats Protected Index (GPHPI) showcases which jurisdictions contribute the most area to the protection of these habitats globally. We also evaluated which jurisdictions have the highest opportunity to contribute globally to protecting habitats by meeting a target of 30% coverage. We found that Areas Beyond National Jurisdiction (ABNJ) have the greatest potential to do so. Our workflow can also be easily extended to terrestrial and freshwater habitats. These indexes are helpful to monitor aspects of the Sustainable Development Goal 14 and the emerging post-2020 global biodiversity framework, to understand the current status of international cooperation on coastal and marine habitats conservation.

Actions to halt biodiversity loss generally benefit the climate.

The two most urgent and interlinked environmental challenges humanity faces are climate change and biodiversity loss. We are entering a pivotal decade for both the international biodiversity and climate change agendas with the sharpening of ambitious strategies and targets by the Convention on Biological Diversity and the United Nations Framework Convention on Climate Change. Within their respective Conventions, the biodiversity and climate interlinked challenges have largely been addressed separately. There is evidence that conservation actions that halt, slow or reverse biodiversity loss can simultaneously slow anthropogenic mediated climate change significantly. This review highlights conservation actions which have the largest potential for mitigation of climate change. We note that conservation actions have mainly synergistic benefits and few antagonistic trade-offs with climate change mitigation. Specifically, we identify direct co-benefits in 14 out of the 21 action targets of the draft post-2020 global biodiversity framework of the Convention on Biological Diversity, notwithstanding the many indirect links that can also support both biodiversity conservation and climate change mitigation. These relationships are context and scale-dependent; therefore, we showcase examples of local biodiversity conservation actions that can be incentivized, guided and prioritized by global objectives and targets. The close interlinkages between biodiversity, climate change mitigation, other nature's contributions to people and good quality of life are seldom as integrated as they should be in management and policy. This review aims to re-emphasize the vital relationships between biodiversity conservation actions and climate change mitigation in a timely manner, in support to major Conferences of Parties that are about to negotiate strategic frameworks and international goals for the decades to come.

How do we best synergize climate mitigation actions to co-benefit biodiversity?

A multitude of actions to protect, sustainably manage and restore natural and modified ecosystems can have co-benefits for both climate mitigation and biodiversity conservation. Reducing greenhouse emissions to limit warming to less than 1.5 or 2°C above preindustrial levels, as outlined in the Paris Agreement, can yield strong co-benefits for land, freshwater and marine biodiversity and reduce amplifying climate feedbacks from ecosystem changes. Not all climate mitigation strategies are equally effective at producing biodiversity co-benefits, some in fact are counterproductive. Moreover, social implications are often overlooked within the climate-biodiversity nexus. Protecting biodiverse and carbon-rich natural environments, ecological restoration of potentially biodiverse and carbon-rich habitats, the deliberate creation of novel habitats, taking into consideration a locally adapted and meaningful (i.e. full consequences considered) mix of these measures, can result in the most robust win-win solutions. These can be further enhanced by avoidance of narrow goals, taking long-term views and minimizing further losses of intact ecosystems. In this review paper, we first discuss various climate mitigation actions that evidence demonstrates can negatively impact biodiversity, resulting in unseen and unintended negative consequences. We then examine climate mitigation actions that co-deliver biodiversity and societal benefits. We give examples of these win-win solutions, categorized as 'protect, restore, manage and create', in different regions of the world that could be expanded, upscaled and used for further innovation.

Fauna of the Kemp Caldera and its upper bathyal hydrothermal vents (South Sandwich Arc, Antarctica).

Faunal assemblages at hydrothermal vents associated with island-arc volcanism are less well known than those at vents on mid-ocean ridges and back-arc spreading centres. This study characterizes chemosynthetic biotopes at active hydrothermal vents discovered at the Kemp Caldera in the South Sandwich Arc. The caldera hosts sulfur and anhydrite vent chimneys in 1375-1487 m depth, which emit sulfide-rich fluids with temperatures up to 212°C, and the microbial community of water samples in the buoyant plume rising from the vents was dominated by sulfur-oxidizing Gammaproteobacteria. A total of 12 macro- and megafaunal taxa depending on hydrothermal activity were collected in these biotopes, of which seven species were known from the East Scotia Ridge (ESR) vents and three species from vents outside the Southern Ocean. Faunal assemblages were dominated by large vesicomyid clams, actinostolid anemones, Sericosura sea spiders and lepetodrilid and cocculinid limpets, but several taxa abundant at nearby ESR hydrothermal vents were rare such as the stalked barnacle Neolepas scotiaensis. Multivariate analysis of fauna at Kemp Caldera and vents in neighbouring areas indicated that the Kemp Caldera is most similar to vent fields in the previously established Southern Ocean vent biogeographic province, showing that the species composition at island-arc hydrothermal vents can be distinct from nearby seafloor-spreading systems. δ 13C and δ 15N isotope values of megafaunal species analysed from the Kemp Caldera were similar to those of the same or related species at other vent fields, but none of the fauna sampled at Kemp Caldera had δ 13C values, indicating nutritional dependence on Epsilonproteobacteria, unlike fauna at other island-arc hydrothermal vents.

Low connectivity between shallow, mesophotic and rariphotic zone benthos.

Worldwide coral reefs face catastrophic damage due to a series of anthropogenic stressors. Investigating how coral reefs ecosystems are connected, in particular across depth, will help us understand if deeper reefs harbour distinct communities. Here, we explore changes in benthic community structure across 15-300 m depths using technical divers and submersibles around Bermuda. We report high levels of floral and faunal differentiation across depth, with distinct assemblages occupying each depth surveyed, except 200-300 m, corresponding to the lower rariphotic zone. Community turnover was highest at the boundary depths of mesophotic coral ecosystems (30-150 m) driven largely by taxonomic turnover and to a lesser degree by ordered species loss (nestedness). Our work highlights the biologically unique nature of benthic communities in the mesophotic and rariphotic zones, and their limited connectivity to shallow reefs, thus emphasizing the need to manage and protect deeper reefs as distinct entities.

Changes in zooplankton communities from epipelagic to lower mesopelagic waters.

Zooplankton form a trophic link between primary producers and higher trophic levels, and exert significant influence on the vertical transport of carbon through the water column ('biological carbon pump'). Using a MultiNet we sampled and studied mesozooplankton communities (i.e. >0.2 mm) from six locations around Bermuda targeting four depth zones: ∼0-200 m, ∼200-400 m, ∼400-600 m (deep-scattering layer), and ∼600-800 m. Copepoda, our focal taxonomic group, consistently dominated samples (∼80% relative abundance). We report declines in zooplankton and copepod abundance with depth, concurrent with decreases in food availability. Taxonomic richness was lowest at depth and below the deep-scattering layer. In contrast, copepod diversity peaked at these depths, suggesting lower competitive displacement in these more food-limited waters. Finally, omnivory and carnivory, were the dominant trophic traits, each one affecting the biological carbon pump in a different way. This highlights the importance of incorporating data on zooplankton food web structure in future modelling of global ocean carbon cycling.

Aggregating behaviour in invasive Caribbean lionfish is driven by habitat complexity.

Caribbean lionfish (Pterois spp.) are considered the most heavily impacting invasive marine vertebrate ever recorded. However, current management is largely inadequate, relying on opportunistic culling by recreational SCUBA divers. Culling efficiency could be greatly improved by exploiting natural aggregations, but to date this behaviour has only been recorded anecdotally, and the drivers are unknown. We found aggregations to be common in situ, but detected no conspecific attraction through visual or olfactory cues in laboratory experiments. Aggregating individuals were on average larger, but showed no further differences in morphology or life history. However, using visual assessments and 3D modelling we show lionfish prefer broad-scale, but avoid fine-scale, habitat complexity. We therefore suggest that lionfish aggregations are coincidental based on individuals' mutual attraction to similar reef structure to maximise hunting efficiency. Using this knowledge, artificial aggregation devices might be developed to concentrate lionfish densities and thus improve culling efficiency.

Investigating the environmental drivers of deep-seafloor biodiversity: A case study of peracarid crustacean assemblages in the Northwest Atlantic Ocean.

The deep-sea benthos covers over 90% of seafloor area and hosts a great diversity of species which contribute toward essential ecosystem services. Evidence suggests that deep-seafloor assemblages are structured predominantly by their physical environment, yet knowledge of assemblage/environment relationships is limited. Here, we utilized a very large dataset of Northwest Atlantic Ocean continental slope peracarid crustacean assemblages as a case study to investigate the environmental drivers of deep-seafloor macrofaunal biodiversity. We investigated biodiversity from a phylogenetic, functional, and taxonomic perspective, and found that a wide variety of environmental drivers, including food availability, physical disturbance (bottom trawling), current speed, sediment characteristics, topographic heterogeneity, and temperature (in order of relative importance), significantly influenced peracarid biodiversity. We also found deep-water peracarid assemblages to vary seasonally and interannually. Contrary to prevailing theory on the drivers of deep-seafloor diversity, we found high topographic heterogeneity (at the hundreds to thousands of meter scale) to negatively influence assemblage diversity, while broadscale sediment characteristics (i.e., percent sand content) were found to influence assemblages more than sediment particle-size diversity. However, our results support other paradigms of deep-seafloor biodiversity, including that assemblages may vary inter- and intra-annually, and how assemblages respond to changes in current speed. We found that bottom trawling negatively affects the evenness and diversity of deep-sea soft-sediment peracarid assemblages, but that predicted changes in ocean temperature as a result of climate change may not strongly influence continental slope biodiversity over human timescales, although it may alter deep-sea community biomass. Finally, we emphasize the value of analyzing multiple metrics of biodiversity and call for researchers to consider an expanded definition of biodiversity in future investigations of deep-ocean life.

Exceptional biodiversity of the cryptofaunal decapods in the Chagos Archipelago, central Indian Ocean.

The Chagos Archipelago is geographically remote and isolated from most direct anthropogenic pressures. Here, we quantify the abundance and diversity of decapod crustaceans inhabiting dead coral colonies, representing a standardised microhabitat, across the Archipelago. Using morphological and molecular techniques we recorded 1868 decapods from 164 nominal species within 54 dead coral colonies, but total species estimates (Chao1 estimator) calculate at least 217 species. Galatheids were the most dominant taxa, though alpheids and hippolytids were also very abundant. 32% of species were rare, and 46% of species were found at only one atoll. This prevalence of rarer species has been reported in other cryptofauna studies, suggesting these assemblages maybe comprised of low-abundance species. This study provides the first estimate of diversity for reef cryptofauna in Chagos, which will serve as a useful baseline for global comparisons of coral reef biodiversity.

Comparative population genomics reveals key barriers to dispersal in Southern Ocean penguins.

The mechanisms that determine patterns of species dispersal are important factors in the production and maintenance of biodiversity. Understanding these mechanisms helps to forecast the responses of species to environmental change. Here, we used a comparative framework and genomewide data obtained through RAD-Seq to compare the patterns of connectivity among breeding colonies for five penguin species with shared ancestry, overlapping distributions and differing ecological niches, allowing an examination of the intrinsic and extrinsic barriers governing dispersal patterns. Our findings show that at-sea range and oceanography underlie patterns of dispersal in these penguins. The pelagic niche of emperor (Aptenodytes forsteri), king (A. patagonicus), Adélie (Pygoscelis adeliae) and chinstrap (P. antarctica) penguins facilitates gene flow over thousands of kilometres. In contrast, the coastal niche of gentoo penguins (P. papua) limits dispersal, resulting in population divergences. Oceanographic fronts also act as dispersal barriers to some extent. We recommend that forecasts of extinction risk incorporate dispersal and that management units are defined by at-sea range and oceanography in species lacking genetic data.

Phylogenetic and functional evidence suggests that deep-ocean ecosystems are highly sensitive to environmental change and direct human disturbance.

An understanding of the balance of interspecific competition and the physical environment in structuring organismal communities is crucial because those communities structured primarily by their physical environment typically exhibit greater sensitivity to environmental change than those structured predominantly by competitive interactions. Here, using detailed phylogenetic and functional information, we investigate this question in macrofaunal assemblages from Northwest Atlantic Ocean continental slopes, a high seas region projected to experience substantial environmental change through the current century. We demonstrate assemblages to be both phylogenetically and functionally under-dispersed, and thus conclude that the physical environment, not competition, may dominate in structuring deep-ocean communities. Further, we find temperature and bottom trawling intensity to be among the environmental factors significantly related to assemblage diversity. These results hint that deep-ocean communities are highly sensitive to their physical environment and vulnerable to environmental perturbation, including by direct disturbance through fishing, and indirectly through the changes brought about by climate change.

The Biology of Seamounts: 25 Years on.

Seamounts are one of the major biomes of the global ocean. The last 25 years of research has seen considerable advances in the understanding of these ecosystems. The interactions between seamounts and steady and variable flows have now been characterised providing a better mechanistic understanding of processes influencing biology. Processes leading to upwelling, including Taylor column formation and tidal rectification, have now been defined as well as those leading to draw down of organic matter from the ocean surface to seamount summit and flanks. There is also an improved understanding of the interactions between seamounts, zooplankton and micronekton communities especially with respect to increased predation pressure in the vicinity of seamounts. Evidence has accumulated of the role of seamounts as hot spots for ocean predators including large pelagic fish, sharks, pinnipeds, cetaceans and seabirds. The complexity of benthic communities associated with seamounts is high and drivers of biodiversity are now being resolved. Claims of high endemism resulting from isolation of seamounts as islands of habitat and speciation have not been supported. However, for species characterised by low dispersal capability, such as some groups of benthic sessile or low-mobility invertebrates, low connectivity between seamount populations has been found with evidence of endemism at a local level. Threats to seamounts have increased in the last 25 years and include overfishing, destructive fishing, marine litter, direct and indirect impacts of climate change and potentially marine mining in the near future. Issues around these threats and their management are discussed.

Trait and phylogenetic diversity provide insights into community assembly of reef-associated shrimps (Palaemonidae) at different spatial scales across the Chagos Archipelago.

Coral reefs are the most biodiverse marine ecosystem and one of the most threatened by global climate change impacts. The vast majority of diversity on reefs is comprised of small invertebrates that live within the reef structure, termed the cryptofauna. This component of biodiversity is hugely understudied, and many species remain undescribed. This study represents a rare analysis of assembly processes structuring a distinct group of cryptofauna, the Palaemonidae, in the Chagos Archipelago, a reef ecosystem under minimal direct human impacts in the central Indian Ocean. The Palaemonidae are a diverse group of Caridae (infraorder of shrimps) that inhabit many different niches on coral reefs and are of particular interest because of their varied habitat associations. Phylogenetic and trait diversity and phylogenetic signal were used to infer likely drivers of community structure. The mechanisms driving palaemonid community assembly and maintenance in the Chagos Archipelago showed distinct spatial patterns. At local scales, among coral colonies and among reefs fringing individual atolls, significant trait, and phylogenetic clustering patterns suggest environmental filtering may be a dominant ecological process driving Palaemonidae community structure, although local competition through equalizing mechanisms may also play a role in shaping the local community structure. Importantly, we also tested the robustness of phylogenetic diversity to changes in evolutionary information as multi-gene phylogenies are resource intensive and for large families, such as the Palaemonidae, are often incomplete. These tests demonstrated a very modest impact on phylogenetic community structure, with only one of the four genes (PEPCK gene) in the phylogeny affecting phylogenetic diversity patterns, which provides useful information for future studies on large families with incomplete phylogenies. These findings contribute to our limited knowledge of this component of biodiversity in a marine locality as close to undisturbed by humans as can be found. It also provides a rare evaluation of phylogenetic diversity methods.

Experimental evidence for reduced mortality of Agaricia lamarcki on a mesophotic reef.

Mesophotic Coral Ecosystems (MCEs) may act as a refuge for impacted shallow reefs as some of the stressors affecting tropical reefs attenuate with depth. A less impacted population at depth could provide recruits to recolonise shallow reefs. Recently, disturbance has been reported on several mesophotic reefs including storm damage, biological invasions, and coral bleaching; calling into question the extent of deep reef refuges. We report on a reciprocal transplant experiment between shallow and mesophotic reefs in the Caribbean, which occurred during a period of coral bleaching. 102 fragments of Agaricia lamarcki were collected down a continuous depth gradient at two sites to a maximum depth of 60m. Fragments were transplanted to either a shallow or mesophotic station at a third site, with controls. This allowed the disaggregation of the effect of the disturbance experienced during the observation period, and any potential acclimation resulting from the historical location of a fragment. Mortality and bleaching were quantitatively assessed. We found the relocation depth of a coral fragment had the strongest effect on both survival and the degree of bleaching recorded. The site a fragment was collected from, and the original collection depth, failed to explain mortality or bleaching with statistical significance. This experiment provides support for the assumption that mesophotic corals may be protected in comparison to shallow reefs, in spite of the potential effects of differing susceptibilities to stress.

Lionfish (Pterois spp.) invade the upper-bathyal zone in the western Atlantic.

Non-native lionfish have been recorded throughout the western Atlantic on both shallow and mesophotic reefs, where they have been linked to declines in reef health. In this study we report the first lionfish observations from the deep sea (>200 m) in Bermuda and Roatan, Honduras, with lionfish observed to a maximum depth of 304 m off the Bermuda platform, and 250 m off West End, Roatan. Placed in the context of other deeper lionfish observations and records, our results imply that lionfish may be present in the 200-300 m depth range of the upper-bathyal zone across many locations in the western Atlantic, but currently are under-sampled compared to shallow habitats. We highlight the need for considering deep-sea lionfish populations in future invasive lionfish management.

Using light-dependent scleractinia to define the upper boundary of mesophotic coral ecosystems on the reefs of Utila, Honduras.

Shallow water zooxanthellate coral reefs grade into ecologically distinct mesophotic coral ecosystems (MCEs) deeper in the euphotic zone. MCEs are widely considered to start at an absolute depth limit of 30m deep, possibly failing to recognise that these are distinct ecological communities that may shift shallower or deeper depending on local environmental conditions. This study aimed to explore whether MCEs represent distinct biological communities, the upper boundary of which can be defined and whether the depth at which they occur may vary above or below 30m. Mixed-gas diving and closed-circuit rebreathers were used to quantitatively survey benthic communities across shallow to mesophotic reef gradients around the island of Utila, Honduras. Depths of up to 85m were sampled, covering the vertical range of the zooxanthellate corals around Utila. We investigate vertical reef zonation using a variety of ecological metrics to identify community shifts with depth, and the appropriateness of different metrics to define the upper MCE boundary. Patterns observed in scleractinian community composition varied between ordination analyses and approaches utilising biodiversity indices. Indices and richness approaches revealed vertical community transition was a gradation. Ordination approaches suggest the possibility of recognising two scleractinian assemblages. We could detect a mesophotic and shallow community while illustrating that belief in a static depth limit is biologically unjustified. The switch between these two communities occurred across bathymetric gradients as small as 10m and as large as 50m in depth. The difference between communities appears to be a loss of shallow specialists and increase in depth-generalist taxa. Therefore, it may be possible to define MCEs by a loss of shallow specialist species. To support a biological definition of mesophotic reefs, we advocate this analytical framework should be applied around the Caribbean and extended into other ocean basins where MCEs are present.

Depth-dependent effects of culling-do mesophotic lionfish populations undermine current management?

Invasive lionfish (Pterois volitans and P. miles) have spread widely across the western Atlantic and are recognized as a major threat to native marine biodiversity. Although lionfish inhabit both shallow reefs and mesophotic coral ecosystems (MCEs; reefs from 30 to 150 m depth), the primary management response implemented by many countries has been diver-led culling limited to reefs less than 30 m. However, many reef fish undergo ontogenetic migrations, with the largest and therefore most fecund individuals found at greatest depths. Here, we study lionfish density, body size, maturity and dietary patterns across the depth gradient from the surface down to 85 m on heavily culled reefs around Utila, Honduras. We found lionfish at increased densities, body size and weight on MCEs compared with shallow reefs, with MCEs also containing the greatest proportion of actively spawning females, while shallow reefs contained the greatest proportion of immature lionfish. We then compared lionfish behaviour in response to divers on shallow culled and mesophotic unculled Utilan reefs, and on shallow unculled reefs in Tela Bay, on the Honduran mainland. We found that mesophotic lionfish exhibited high alert distances, consistent with individuals previously exposed to culling despite being below the depth limits of removal. In addition, when examining stomach content, we found that fish were the major component of lionfish diets across the depth gradient. Importantly, our results suggest that despite adjacent shallow culling, MCEs retain substantial lionfish populations that may be disproportionately contributing towards continued lionfish recruitment onto the shallow reefs of Utila, potentially undermining current culling-based management.

The challenges of detecting subtle population structure and its importance for the conservation of emperor penguins.

Understanding the boundaries of breeding populations is of great importance for conservation efforts and estimates of extinction risk for threatened species. However, determining these boundaries can be difficult when population structure is subtle. Emperor penguins are highly reliant on sea ice, and some populations may be in jeopardy as climate change alters sea-ice extent and quality. An understanding of emperor penguin population structure is therefore urgently needed. Two previous studies have differed in their conclusions, particularly whether the Ross Sea, a major stronghold for the species, is isolated or not. We assessed emperor penguin population structure using 4,596 genome-wide single nucleotide polymorphisms (SNPs), characterized in 110 individuals (10-16 per colony) from eight colonies around Antarctica. In contrast to a previous conclusion that emperor penguins are panmictic around the entire continent, we find that emperor penguins comprise at least four metapopulations, and that the Ross Sea is clearly a distinct metapopulation. Using larger sample sizes and a thorough assessment of the limitations of different analytical methods, we have shown that population structure within emperor penguins does exist and argue that its recognition is vital for the effective conservation of the species. We discuss the many difficulties that molecular ecologists and managers face in the detection and interpretation of subtle population structure using large SNP data sets, and argue that subtle structure should be taken into account when determining management strategies for threatened species, until accurate estimates of demographic connectivity among populations can be made.