Past and future decline of tropical pelagic biodiversity.

A major research question concerning global pelagic biodiversity remains unanswered: when did the apparent tropical biodiversity depression (i.e., bimodality of latitudinal diversity gradient [LDG]) begin? The bimodal LDG may be a consequence of recent ocean warming or of deep-time evolutionary speciation and extinction processes. Using rich fossil datasets of planktonic foraminifers, we show here that a unimodal (or only weakly bimodal) diversity gradient, with a plateau in the tropics, occurred during the last ice age and has since then developed into a bimodal gradient through species distribution shifts driven by postglacial ocean warming. The bimodal LDG likely emerged before the Anthropocene and industrialization, and perhaps ∼15,000 y ago, indicating a strong environmental control of tropical diversity even before the start of anthropogenic warming. However, our model projections suggest that future anthropogenic warming further diminishes tropical pelagic diversity to a level not seen in millions of years.

Deep-sea diversity patterns are shaped by energy availability.

The deep ocean is the largest and least-explored ecosystem on Earth, and a uniquely energy-poor environment. The distribution, drivers and origins of deep-sea biodiversity remain unknown at global scales. Here we analyse a database of more than 165,000 distribution records of Ophiuroidea (brittle stars), a dominant component of sea-floor fauna, and find patterns of biodiversity unlike known terrestrial or coastal marine realms. Both patterns and environmental predictors of deep-sea (2,000-6,500 m) species richness fundamentally differ from those found in coastal (0-20 m), continental shelf (20-200 m), and upper-slope (200-2,000 m) waters. Continental shelf to upper-slope richness consistently peaks in tropical Indo-west Pacific and Caribbean (0-30°) latitudes, and is well explained by variations in water temperature. In contrast, deep-sea species show maximum richness at higher latitudes (30-50°), concentrated in areas of high carbon export flux and regions close to continental margins. We reconcile this structuring of oceanic biodiversity using a species-energy framework, with kinetic energy predicting shallow-water richness, while chemical energy (export productivity) and proximity to slope habitats drive deep-sea diversity. Our findings provide a global baseline for conservation efforts across the sea floor, and demonstrate that deep-sea ecosystems show a biodiversity pattern consistent with ecological theory, despite being different from other planetary-scale habitats.

Global ensemble projections reveal trophic amplification of ocean biomass declines with climate change.

While the physical dimensions of climate change are now routinely assessed through multimodel intercomparisons, projected impacts on the global ocean ecosystem generally rely on individual models with a specific set of assumptions. To address these single-model limitations, we present standardized ensemble projections from six global marine ecosystem models forced with two Earth system models and four emission scenarios with and without fishing. We derive average biomass trends and associated uncertainties across the marine food web. Without fishing, mean global animal biomass decreased by 5% (±4% SD) under low emissions and 17% (±11% SD) under high emissions by 2100, with an average 5% decline for every 1 °C of warming. Projected biomass declines were primarily driven by increasing temperature and decreasing primary production, and were more pronounced at higher trophic levels, a process known as trophic amplification. Fishing did not substantially alter the effects of climate change. Considerable regional variation featured strong biomass increases at high latitudes and decreases at middle to low latitudes, with good model agreement on the direction of change but variable magnitude. Uncertainties due to variations in marine ecosystem and Earth system models were similar. Ensemble projections performed well compared with empirical data, emphasizing the benefits of multimodel inference to project future outcomes. Our results indicate that global ocean animal biomass consistently declines with climate change, and that these impacts are amplified at higher trophic levels. Next steps for model development include dynamic scenarios of fishing, cumulative human impacts, and the effects of management measures on future ocean biomass trends.

Incorporating climate change adaptation into marine protected area planning.

Climate change is increasingly impacting marine protected areas (MPAs) and MPA networks, yet adaptation strategies are rarely incorporated into MPA design and management plans according to the primary scientific literature. Here we review the state of knowledge for adapting existing and future MPAs to climate change and synthesize case studies (n = 27) of how marine conservation planning can respond to shifting environmental conditions. First, we derive a generalized conservation planning framework based on five published frameworks that incorporate climate change adaptation to inform MPA design. We then summarize examples from the scientific literature to assess how conservation goals were defined, vulnerability assessments performed and adaptation strategies incorporated into the design and management of existing or new MPAs. Our analysis revealed that 82% of real-world examples of climate change adaptation in MPA planning derive from tropical reefs, highlighting the need for research in other ecosystems and habitat types. We found contrasting recommendations for adaptation strategies at the planning stage, either focusing only on climate refugia, or aiming for representative protection of areas encompassing the full range of expected climate change impacts. Recommendations for MPA management were more unified and focused on adaptative management approaches. Lastly, we evaluate common barriers to adopting climate change adaptation strategies based on reviewing studies which conducted interviews with MPA managers and other conservation practitioners. This highlights a lack of scientific studies evaluating different adaptation strategies and shortcomings in current governance structures as two major barriers, and we discuss how these could be overcome. Our review provides a comprehensive synthesis of planning frameworks, case studies, adaptation strategies and management actions which can inform a more coordinated global effort to adapt existing and future MPA networks to continued climate change.

Twenty-first-century climate change impacts on marine animal biomass and ecosystem structure across ocean basins.

Climate change effects on marine ecosystems include impacts on primary production, ocean temperature, species distributions, and abundance at local to global scales. These changes will significantly alter marine ecosystem structure and function with associated socio-economic impacts on ecosystem services, marine fisheries, and fishery-dependent societies. Yet how these changes may play out among ocean basins over the 21st century remains unclear, with most projections coming from single ecosystem models that do not adequately capture the range of model uncertainty. We address this by using six marine ecosystem models within the Fisheries and Marine Ecosystem Model Intercomparison Project (Fish-MIP) to analyze responses of marine animal biomass in all major ocean basins to contrasting climate change scenarios. Under a high emissions scenario (RCP8.5), total marine animal biomass declined by an ensemble mean of 15%-30% (±12%-17%) in the North and South Atlantic and Pacific, and the Indian Ocean by 2100, whereas polar ocean basins experienced a 20%-80% (±35%-200%) increase. Uncertainty and model disagreement were greatest in the Arctic and smallest in the South Pacific Ocean. Projected changes were reduced under a low (RCP2.6) emissions scenario. Under RCP2.6 and RCP8.5, biomass projections were highly correlated with changes in net primary production and negatively correlated with projected sea surface temperature increases across all ocean basins except the polar oceans. Ecosystem structure was projected to shift as animal biomass concentrated in different size-classes across ocean basins and emissions scenarios. We highlight that climate change mitigation measures could moderate the impacts on marine animal biomass by reducing biomass declines in the Pacific, Atlantic, and Indian Ocean basins. The range of individual model projections emphasizes the importance of using an ensemble approach in assessing uncertainty of future change.

Emergent global patterns of ecosystem structure and function from a mechanistic general ecosystem model.

Anthropogenic activities are causing widespread degradation of ecosystems worldwide, threatening the ecosystem services upon which all human life depends. Improved understanding of this degradation is urgently needed to improve avoidance and mitigation measures. One tool to assist these efforts is predictive models of ecosystem structure and function that are mechanistic: based on fundamental ecological principles. Here we present the first mechanistic General Ecosystem Model (GEM) of ecosystem structure and function that is both global and applies in all terrestrial and marine environments. Functional forms and parameter values were derived from the theoretical and empirical literature where possible. Simulations of the fate of all organisms with body masses between 10 µg and 150,000 kg (a range of 14 orders of magnitude) across the globe led to emergent properties at individual (e.g., growth rate), community (e.g., biomass turnover rates), ecosystem (e.g., trophic pyramids), and macroecological scales (e.g., global patterns of trophic structure) that are in general agreement with current data and theory. These properties emerged from our encoding of the biology of, and interactions among, individual organisms without any direct constraints on the properties themselves. Our results indicate that ecologists have gathered sufficient information to begin to build realistic, global, and mechanistic models of ecosystems, capable of predicting a diverse range of ecosystem properties and their response to human pressures.

Synergistic impacts of habitat loss and fragmentation on model ecosystems.

Habitat loss and fragmentation are major threats to biodiversity, yet separating their effects is challenging. We use a multi-trophic, trait-based, and spatially explicit general ecosystem model to examine the independent and synergistic effects of these processes on ecosystem structure. We manipulated habitat by removing plant biomass in varying spatial extents, intensities, and configurations. We found that emergent synergistic interactions of loss and fragmentation are major determinants of ecosystem response, including population declines and trophic pyramid shifts. Furthermore, trait-mediated interactions, such as a disproportionate sensitivity of large-sized organisms to fragmentation, produce significant effects in shaping responses. We also show that top-down regulation mitigates the effects of land use on plant biomass loss, suggesting that models lacking these interactions-including most carbon stock models-may not adequately capture land-use change impacts. Our results have important implications for understanding ecosystem responses to environmental change, and assessing the impacts of habitat fragmentation.

Global patterns and predictors of marine biodiversity across taxa.

Global patterns of species richness and their structuring forces have fascinated biologists since Darwin and provide critical context for contemporary studies in ecology, evolution and conservation. Anthropogenic impacts and the need for systematic conservation planning have further motivated the analysis of diversity patterns and processes at regional to global scales. Whereas land diversity patterns and their predictors are known for numerous taxa, our understanding of global marine diversity has been more limited, with recent findings revealing some striking contrasts to widely held terrestrial paradigms. Here we examine global patterns and predictors of species richness across 13 major species groups ranging from zooplankton to marine mammals. Two major patterns emerged: coastal species showed maximum diversity in the Western Pacific, whereas oceanic groups consistently peaked across broad mid-latitudinal bands in all oceans. Spatial regression analyses revealed sea surface temperature as the only environmental predictor highly related to diversity across all 13 taxa. Habitat availability and historical factors were also important for coastal species, whereas other predictors had less significance. Areas of high species richness were disproportionately concentrated in regions with medium or higher human impacts. Our findings indicate a fundamental role of temperature or kinetic energy in structuring cross-taxon marine biodiversity, and indicate that changes in ocean temperature, in conjunction with other human impacts, may ultimately rearrange the global distribution of life in the ocean.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

Energetics of life on the deep seafloor.

With frigid temperatures and virtually no in situ productivity, the deep oceans, Earth's largest ecosystem, are especially energy-deprived systems. Our knowledge of the effects of this energy limitation on all levels of biological organization is very incomplete. Here, we use the Metabolic Theory of Ecology to examine the relative roles of carbon flux and temperature in influencing metabolic rate, growth rate, lifespan, body size, abundance, biomass, and biodiversity for life on the deep seafloor. We show that the relative impacts of thermal and chemical energy change across organizational scales. Results suggest that individual metabolic rates, growth, and turnover proceed as quickly as temperature-influenced biochemical kinetics allow but that chemical energy limits higher-order community structure and function. Understanding deep-sea energetics is a pressing problem because of accelerating climate change and the general lack of environmental regulatory policy for the deep oceans.

How many species are there on Earth and in the ocean?

The diversity of life is one of the most striking aspects of our planet; hence knowing how many species inhabit Earth is among the most fundamental questions in science. Yet the answer to this question remains enigmatic, as efforts to sample the world's biodiversity to date have been limited and thus have precluded direct quantification of global species richness, and because indirect estimates rely on assumptions that have proven highly controversial. Here we show that the higher taxonomic classification of species (i.e., the assignment of species to phylum, class, order, family, and genus) follows a consistent and predictable pattern from which the total number of species in a taxonomic group can be estimated. This approach was validated against well-known taxa, and when applied to all domains of life, it predicts ~8.7 million (± 1.3 million SE) eukaryotic species globally, of which ~2.2 million (± 0.18 million SE) are marine. In spite of 250 years of taxonomic classification and over 1.2 million species already catalogued in a central database, our results suggest that some 86% of existing species on Earth and 91% of species in the ocean still await description. Renewed interest in further exploration and taxonomy is required if this significant gap in our knowledge of life on Earth is to be closed.

Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes.

Difficulties in scaling up theoretical and experimental results have raised controversy over the consequences of biodiversity loss for the functioning of natural ecosystems. Using a global survey of reef fish assemblages, we show that in contrast to previous theoretical and experimental studies, ecosystem functioning (as measured by standing biomass) scales in a non-saturating manner with biodiversity (as measured by species and functional richness) in this ecosystem. Our field study also shows a significant and negative interaction between human population density and biodiversity on ecosystem functioning (i.e., for the same human density there were larger reductions in standing biomass at more diverse reefs). Human effects were found to be related to fishing, coastal development, and land use stressors, and currently affect over 75% of the world's coral reefs. Our results indicate that the consequences of biodiversity loss in coral reefs have been considerably underestimated based on existing knowledge and that reef fish assemblages, particularly the most diverse, are greatly vulnerable to the expansion and intensity of anthropogenic stressors in coastal areas.

Range contraction in large pelagic predators.

Large reductions in the abundance of exploited land predators have led to significant range contractions for those species. This pattern can be formalized as the range-abundance relationship, a general macroecological pattern that has important implications for the conservation of threatened species. Here we ask whether similar responses may have occurred in highly mobile pelagic predators, specifically 13 species of tuna and billfish. We analyzed two multidecadal global data sets on the spatial distribution of catches and fishing effort targeting these species and compared these with available abundance time series from stock assessments. We calculated the effort needed to reliably detect the presence of a species and then computed observed range sizes in each decade from 1960 to 2000. Results suggest significant range contractions in 9 of the 13 species considered here (between 2% and 46% loss of observed range) and significant range expansions in two species (11-29% increase). Species that have undergone the largest declines in abundance and are of particular conservation concern tended to show the largest range contractions. These include all three species of bluefin tuna and several marlin species. In contrast, skipjack tuna, which may have increased its abundance in the Pacific, has also expanded its range size. These results mirror patterns described for many land predators, despite considerable differences in habitat, mobility, and dispersal, and imply ecological extirpation of heavily exploited species across parts of their range.

A database of mapped global fishing activity 1950-2017.

A new database on historical country-level fishing fleet capacity and effort is described, derived from a range of publicly available sources that were harmonized, converted to fishing effort, and mapped to 30-min spatial cells. The resulting data is comparable with widely used but more temporally-limited satellite-sourced Automatic Identification System (AIS) datasets for large vessels, while also documenting important smaller fleets and artisanal segments. It ranges from 1950 to 2017, and includes information on number of vessels, engine power, gross tonnage, and nominal effort, categorized by vessel length, gear type and targeted functional groups. The data can be aggregated to Large Marine Ecosystem, region and/or fishing country scales and provides a temporally and spatially explicit source for fishing effort and fleet capacity for studies aimed at understanding the implications of long-term changes in fishing activity in the global ocean.

Trophic amplification: A model intercomparison of climate driven changes in marine food webs.

Marine animal biomass is expected to decrease in the 21st century due to climate driven changes in ocean environmental conditions. Previous studies suggest that the magnitude of the decline in primary production on apex predators could be amplified through the trophodynamics of marine food webs, leading to larger decreases in the biomass of predators relative to the decrease in primary production, a mechanism called trophic amplification. We compared relative changes in producer and consumer biomass or production in the global ocean to assess the extent of trophic amplification. We used simulations from nine marine ecosystem models (MEMs) from the Fisheries and Marine Ecosystem Models Intercomparison Project forced by two Earth System Models under the high greenhouse gas emissions Shared Socioeconomic Pathways (SSP5-8.5) and a scenario of no fishing. Globally, total consumer biomass is projected to decrease by 16.7 ± 9.5% more than net primary production (NPP) by 2090-2099 relative to 1995-2014, with substantial variations among MEMs and regions. Total consumer biomass is projected to decrease almost everywhere in the ocean (80% of the world's oceans) in the model ensemble. In 40% of the world's oceans, consumer biomass was projected to decrease more than NPP. Additionally, in another 36% of the world's oceans consumer biomass is expected to decrease even as projected NPP increases. By analysing the biomass response within food webs in available MEMs, we found that model parameters and structures contributed to more complex responses than a consistent amplification of climate impacts of higher trophic levels. Our study provides additional insights into the ecological mechanisms that will impact marine ecosystems, thereby informing model and scenario development.

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.