Using the Fossil Record to Understand Extinction Risk and Inform Marine Conservation in a Changing World.

Understanding the long-term effects of ongoing global environmental change on marine ecosystems requires a cross-disciplinary approach. Deep-time and recent fossil records can contribute by identifying traits and environmental conditions associated with elevated extinction risk during analogous events in the geologic past and by providing baseline data that can be used to assess historical change and set management and restoration targets and benchmarks. Here, we review the ecological and environmental information available in the marine fossil record and discuss how these archives can be used to inform current extinction risk assessments as well as marine conservation strategies and decision-making at global to local scales. As we consider future research directions in deep-time and conservationpaleobiology, we emphasize the need for coproduced research that unites researchers, conservation practitioners, and policymakers with the communities for whom the impacts of climate and global change are most imminent.

Next-generation ensemble projections reveal higher climate risks for marine ecosystems.

Projections of climate change impacts on marine ecosystems have revealed long-term declines in global marine animal biomass and unevenly distributed impacts on fisheries. Here we apply an enhanced suite of global marine ecosystem models from the Fisheries and Marine Ecosystem Model Intercomparison Project (Fish-MIP), forced by new-generation Earth system model outputs from Phase 6 of the Coupled Model Intercomparison Project (CMIP6), to provide insights into how projected climate change will affect future ocean ecosystems. Compared with the previous generation CMIP5-forced Fish-MIP ensemble, the new ensemble ecosystem simulations show a greater decline in mean global ocean animal biomass under both strong-mitigation and high-emissions scenarios due to elevated warming, despite greater uncertainty in net primary production in the high-emissions scenario. Regional shifts in the direction of biomass changes highlight the continued and urgent need to reduce uncertainty in the projected responses of marine ecosystems to climate change to help support adaptation planning.

Marine biodiversity conservation.

Marine biodiversity is the essential foundation for the structure and functioning of ocean ecosystems and for providing the full range of ecosystem services that benefit humans on local, regional, and global scales. These benefits include many visible as well as unseen functions and services such as the oxygen we breathe, the seafood we eat, the support of local livelihoods, the marine plants storing 'blue' carbon and protecting our shorelines, the medical and biochemical compounds found in marine species, the coral reefs we explore when scuba diving, and the charismatic creatures inspiring our lives. All these benefits are provided by the diversity and interplay of ocean life, from tiny plankton and bacteria to 30 metre whales and giant kelp.

Future ocean biomass losses may widen socioeconomic equity gaps.

Future climate impacts and their consequences are increasingly being explored using multi-model ensembles that average across individual model projections. Here we develop a statistical framework that integrates projections from coupled ecosystem and earth-system models to evaluate significance and uncertainty in marine animal biomass changes over the 21st century in relation to socioeconomic indicators at national to global scales. Significant biomass changes are projected in 40%-57% of the global ocean, with 68%-84% of these areas exhibiting declining trends under low and high emission scenarios, respectively. Given unabated emissions, maritime nations with poor socioeconomic statuses such as low nutrition, wealth, and ocean health will experience the greatest projected losses. These findings suggest that climate-driven biomass changes will widen existing equity gaps and disproportionally affect populations that contributed least to global CO2 emissions. However, our analysis also suggests that such deleterious outcomes are largely preventable by achieving negative emissions (RCP 2.6).

Rebuilding marine life.

Sustainable Development Goal 14 of the United Nations aims to "conserve and sustainably use the oceans, seas and marine resources for sustainable development". Achieving this goal will require rebuilding the marine life-support systems that deliver the many benefits that society receives from a healthy ocean. Here we document the recovery of marine populations, habitats and ecosystems following past conservation interventions. Recovery rates across studies suggest that substantial recovery of the abundance, structure and function of marine life could be achieved by 2050, if major pressures-including climate change-are mitigated. Rebuilding marine life represents a doable Grand Challenge for humanity, an ethical obligation and a smart economic objective to achieve a sustainable future.

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.

Integrating climate adaptation and biodiversity conservation in the global ocean.

The impacts of climate change and the socioecological challenges they present are ubiquitous and increasingly severe. Practical efforts to operationalize climate-responsive design and management in the global network of marine protected areas (MPAs) are required to ensure long-term effectiveness for safeguarding marine biodiversity and ecosystem services. Here, we review progress in integrating climate change adaptation into MPA design and management and provide eight recommendations to expedite this process. Climate-smart management objectives should become the default for all protected areas, and made into an explicit international policy target. Furthermore, incentives to use more dynamic management tools would increase the climate change responsiveness of the MPA network as a whole. Given ongoing negotiations on international conservation targets, now is the ideal time to proactively reform management of the global seascape for the dynamic climate-biodiversity reality.

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.

State-of-the-art global models underestimate impacts from climate extremes.

Global impact models represent process-level understanding of how natural and human systems may be affected by climate change. Their projections are used in integrated assessments of climate change. Here we test, for the first time, systematically across many important systems, how well such impact models capture the impacts of extreme climate conditions. Using the 2003 European heat wave and drought as a historical analogue for comparable events in the future, we find that a majority of models underestimate the extremeness of impacts in important sectors such as agriculture, terrestrial ecosystems, and heat-related human mortality, while impacts on water resources and hydropower are overestimated in some river basins; and the spread across models is often large. This has important implications for economic assessments of climate change impacts that rely on these models. It also means that societal risks from future extreme events may be greater than previously thought.

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.

Potential impacts of finfish aquaculture on eelgrass (Zostera marina) beds and possible monitoring metrics for management: a case study in Atlantic Canada.

Eelgrass (Zostera marina) has been designated an Ecologically Significant Species in Atlantic Canada. The development and rapid expansion of netpen finfish aquaculture into sensitive coastal habitats has raised concerns about the impacts of finfish aquaculture on eelgrass habitats. To date, no studies have been done in Atlantic Canada to examine these impacts or to identify potential monitoring variables that would aid in the development of specific conservation and management objectives. As a first step in addressing this gap, we examined differences in environmental variables, eelgrass bed structure and macroinfauna communities at increasing distances from a finfish farm in Port Mouton Bay, a reference site in adjacent Port Joli Bay, and published survey results from other sites without finfish farms along the Atlantic Coast of Nova Scotia. Drawing on research done elsewhere and our results, we then identified possible metrics for assessing and monitoring local impacts of finfish aquaculture on eelgrass habitats. Our results suggest some nutrient and organic enrichment, higher epiphyte loads, lower eelgrass cover and biomass, and lower macroinfauna biomass closer to the farm. Moreover, community structure significantly differed between sites with some species increasing and others decreasing closer to the farm. Changes in the macroinfauna community could be linked to observed differences in environmental and eelgrass bed variables. These results provide new insights into the potential impacts of finfish aquaculture on eelgrass habitats in Atlantic Canada. We recommend a suite of measures for assessment and monitoring that take into account response time to disturbance and account for different levels of eelgrass organizational response (from physiological to community).

Linked sustainability challenges and trade-offs among fisheries, aquaculture and agriculture.

Fisheries and aquaculture make a crucial contribution to global food security, nutrition and livelihoods. However, the UN Sustainable Development Goals separate marine and terrestrial food production sectors and ecosystems. To sustainably meet increasing global demands for fish, the interlinkages among goals within and across fisheries, aquaculture and agriculture sectors must be recognized and addressed along with their changing nature. Here, we assess and highlight development challenges for fisheries-dependent countries based on analyses of interactions and trade-offs between goals focusing on food, biodiversity and climate change. We demonstrate that some countries are likely to face double jeopardies in both fisheries and agriculture sectors under climate change. The strategies to mitigate these risks will be context-dependent, and will need to directly address the trade-offs among Sustainable Development Goals, such as halting biodiversity loss and reducing poverty. Countries with low adaptive capacity but increasing demand for food require greater support and capacity building to transition towards reconciling trade-offs. Necessary actions are context-dependent and include effective governance, improved management and conservation, maximizing societal and environmental benefits from trade, increased equitability of distribution and innovation in food production, including continued development of low input and low impact aquaculture.

Critical factors for the recovery of marine mammals.

{en} Over the past decades, much research has focused on understanding the critical factors for marine extinctions with the aim of preventing further species losses in the oceans. Although conservation and management strategies are enabling several species and populations to recover, others remain at low abundance levels or continue to decline. To understand these discrepancies, we used a published database on abundance trends of 137 populations of marine mammals worldwide and compiled data on 28 potentially critical factors for recovery. We then applied random forests and additive mixed models to determine which intrinsic and extrinsic factors are critical for the recovery of marine mammals. A mix of life-history characteristics, ecological traits, phylogenetic relatedness, population size, geographic range, human impacts, and management efforts explained why populations recovered or not. Consistently, species with lower age at maturity and intermediate habitat area were more likely to recover, which is consistent with life-history and ecological theory. Body size, trophic level, social interactions, dominant habitat, ocean basin, and habitat disturbance also explained some differences in recovery patterns. Overall, a variety of intrinsic and extrinsic factors were important for species' recovery, pointing to cumulative effects. Our results provide insight for improving conservation and management strategies to enhance recoveries in the future.

Comparative analysis of different survey methods for monitoring fish assemblages in coastal habitats.

Coastal ecosystems are among the most productive yet increasingly threatened marine ecosystems worldwide. Particularly vegetated habitats, such as eelgrass (Zostera marina) beds, play important roles in providing key spawning, nursery and foraging habitats for a wide range of fauna. To properly assess changes in coastal ecosystems and manage these critical habitats, it is essential to develop sound monitoring programs for foundation species and associated assemblages. Several survey methods exist, thus understanding how different methods perform is important for survey selection. We compared two common methods for surveying macrofaunal assemblages: beach seine netting and underwater visual census (UVC). We also tested whether assemblages in shallow nearshore habitats commonly sampled by beach seines are similar to those of nearby eelgrass beds often sampled by UVC. Among five estuaries along the Southern Gulf of St. Lawrence, Canada, our results suggest that the two survey methods yield comparable results for species richness, diversity and evenness, yet beach seines yield significantly higher abundance and different species composition. However, sampling nearshore assemblages does not represent those in eelgrass beds despite considerable overlap and close proximity. These results have important implications for how and where macrofaunal assemblages are monitored in coastal ecosystems. Ideally, multiple survey methods and locations should be combined to complement each other in assessing the entire assemblage and full range of changes in coastal ecosystems, thereby better informing coastal zone management.

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.

Extinctions. Paleontological baselines for evaluating extinction risk in the modern oceans.

Marine taxa are threatened by anthropogenic impacts, but knowledge of their extinction vulnerabilities is limited. The fossil record provides rich information on past extinctions that can help predict biotic responses. We show that over 23 million years, taxonomic membership and geographic range size consistently explain a large proportion of extinction risk variation in six major taxonomic groups. We assess intrinsic risk-extinction risk predicted by paleontologically calibrated models-for modern genera in these groups. Mapping the geographic distribution of these genera identifies coastal biogeographic provinces where fauna with high intrinsic risk are strongly affected by human activity or climate change. Such regions are disproportionately in the tropics, raising the possibility that these ecosystems may be particularly vulnerable to future extinctions. Intrinsic risk provides a prehuman baseline for considering current threats to marine biodiversity.

Predator decline leads to decreased stability in a coastal fish community.

Fisheries exploitation has caused widespread declines in marine predators. Theory predicts that predator depletion will destabilise lower trophic levels, making natural communities more vulnerable to environmental perturbations. However, empirical evidence has been limited. Using a community matrix model, we empirically assessed trends in the stability of a multispecies coastal fish community over the course of predator depletion. Three indices of community stability (resistance, resilience and reactivity) revealed significantly decreasing stability concurrent with declining predator abundance. The trophically downgraded community exhibited weaker top-down control, leading to predator-release processes in lower trophic levels and increased susceptibility to perturbation. At the community level, our results suggest that high predator abundance acts as a stabilising force to the naturally stochastic and highly autocorrelated dynamics in low trophic species. These findings have important implications for the conservation and management of predators in marine ecosystems and provide empirical support for the theory of predatory control.

Recovery trends in marine mammal populations.

Marine mammals have greatly benefitted from a shift from resource exploitation towards conservation. Often lauded as symbols of conservation success, some marine mammal populations have shown remarkable recoveries after severe depletions. Others have remained at low abundance levels, continued to decline, or become extinct or extirpated. Here we provide a quantitative assessment of (1) publicly available population-level abundance data for marine mammals worldwide, (2) abundance trends and recovery status, and (3) historic population decline and recent recovery. We compiled 182 population abundance time series for 47 species and identified major data gaps. In order to compare across the largest possible set of time series with varying data quality, quantity and frequency, we considered an increase in population abundance as evidence of recovery. Using robust log-linear regression over three generations, we were able to classify abundance trends for 92 spatially non-overlapping populations as Significantly Increasing (42%), Significantly Decreasing (10%), Non-Significant Change (28%) and Unknown (20%). Our results were comparable to IUCN classifications for equivalent species. Among different groupings, pinnipeds and other marine mammals (sirenians, polar bears and otters) showed the highest proportion of recovering populations, likely benefiting from relatively fast life histories and nearshore habitats that provided visibility and protective management measures. Recovery was less frequent among cetaceans, but more common in coastal than offshore populations. For marine mammals with available historical abundance estimates (n = 47), larger historical population declines were associated with low or variable recent recoveries so far. Overall, our results show that many formerly depleted marine mammal populations are recovering. However, data-deficient populations and those with decreasing and non-significant trends require attention. In particular, increased study of populations with major data gaps, including offshore small cetaceans, cryptic species, and marine mammals in low latitudes and developing nations, is needed to better understand the status of marine mammal populations worldwide.

Long-term change in a meso-predator community in response to prolonged and heterogeneous human impact.

Sharks and rays' abundance can decline considerably with fishing. Community changes, however, are more complex because of species interactions, and variable vulnerability and exposure to fishing. We evaluated long-term changes in the elasmobranch community of the Adriatic Sea, a heavily exploited Mediterranean basin where top-predators have been strongly depleted historically, and fishing developed unevenly between the western and eastern side. Combining and standardizing catch data from five trawl surveys from 1948-2005, we estimated abundance trends and explained community changes using life histories, fish-market and effort data, and historical information. We identified a highly depleted elasmobranch community. Since 1948, catch rates have declined by >94% and 11 species ceased to be detected. The exploitation history and spatial gradients in fishing pressure explained most patterns in abundance and diversity, including the absence of strong compensatory increases. Ecological corridors and large-scale protected areas emerged as potential management options for elasmobranch conservation.