A metric-based framework for climate-smart conservation planning.

Climate change is already having profound effects on biodiversity, but climate change adaptation has yet to be fully incorporated into area-based management tools used to conserve biodiversity, such as protected areas. One main obstacle is the lack of consensus regarding how impacts of climate change can be included in spatial conservation plans. We propose a climate-smart framework that prioritizes the protection of climate refugia-areas of low climate exposure and high biodiversity retention-using climate metrics. We explore four aspects of climate-smart conservation planning: (1) climate model ensembles; (2) multiple emission scenarios; (3) climate metrics; and (4) approaches to identifying climate refugia. We illustrate this framework in the Western Pacific Ocean, but it is equally applicable to terrestrial systems. We found that all aspects of climate-smart conservation planning considered affected the configuration of spatial plans. The choice of climate metrics and approaches to identifying refugia have large effects in the resulting climate-smart spatial plans, whereas the choice of climate models and emission scenarios have smaller effects. As the configuration of spatial plans depended on climate metrics used, a spatial plan based on a single measure of climate change (e.g., warming) will not necessarily be robust against other measures of climate change (e.g., ocean acidification). We therefore recommend using climate metrics most relevant for the biodiversity and region considered based on a single or multiple climate drivers. To include the uncertainty associated with different climate futures, we recommend using multiple climate models (i.e., an ensemble) and emission scenarios. Finally, we show that the approaches we used to identify climate refugia feature trade-offs between: (1) the degree to which they are climate-smart, and (2) their efficiency in meeting conservation targets. Hence, the choice of approach will depend on the relative value that stakeholders place on climate adaptation. By using this framework, protected areas can be designed with improved longevity and thus safeguard biodiversity against current and future climate change. We hope that the proposed climate-smart framework helps transition conservation planning toward climate-smart approaches.

Climate change disrupts core habitats of marine species.

Driven by climate change, marine biodiversity is undergoing a phase of rapid change that has proven to be even faster than changes observed in terrestrial ecosystems. Understanding how these changes in species composition will affect future marine life is crucial for conservation management, especially due to increasing demands for marine natural resources. Here, we analyse predictions of a multiparameter habitat suitability model covering the global projected ranges of >33,500 marine species from climate model projections under three CO2 emission scenarios (RCP2.6, RCP4.5, RCP8.5) up to the year 2100. Our results show that the core habitat area will decline for many species, resulting in a net loss of 50% of the core habitat area for almost half of all marine species in 2100 under the high-emission scenario RCP8.5. As an additional consequence of the continuing distributional reorganization of marine life, gaps around the equator will appear for 8% (RCP2.6), 24% (RCP4.5), and 88% (RCP8.5) of marine species with cross-equatorial ranges. For many more species, continuous distributional ranges will be disrupted, thus reducing effective population size. In addition, high invasion rates in higher latitudes and polar regions will lead to substantial changes in the ecosystem and food web structure, particularly regarding the introduction of new predators. Overall, our study highlights that the degree of spatial and structural reorganization of marine life with ensued consequences for ecosystem functionality and conservation efforts will critically depend on the realized greenhouse gas emission pathway.

A functional vulnerability framework for biodiversity conservation.

Setting appropriate conservation strategies in a multi-threat world is a challenging goal, especially because of natural complexity and budget limitations that prevent effective management of all ecosystems. Safeguarding the most threatened ecosystems requires accurate and integrative quantification of their vulnerability and their functioning, particularly the potential loss of species trait diversity which imperils their functioning. However, the magnitude of threats and associated biological responses both have high uncertainties. Additionally, a major difficulty is the recurrent lack of reference conditions for a fair and operational measurement of vulnerability. Here, we present a functional vulnerability framework that incorporates uncertainty and reference conditions into a generalizable tool. Through in silico simulations of disturbances, our framework allows us to quantify the vulnerability of communities to a wide range of threats. We demonstrate the relevance and operationality of our framework, and its global, scalable and quantitative comparability, through three case studies on marine fishes and mammals. We show that functional vulnerability has marked geographic and temporal patterns. We underline contrasting contributions of species richness and functional redundancy to the level of vulnerability among case studies, indicating that our integrative assessment can also identify the drivers of vulnerability in a world where uncertainty is omnipresent.

4D marine conservation networks: Combining 3D prioritization of present and future biodiversity with climatic refugia.

Given the accelerating rate of biodiversity loss, the need to prioritize marine areas for protection represents a major conservation challenge. The three-dimensionality of marine life and ecosystems is an inherent element of complexity for setting spatial conservation plans. Yet, the confidence of any recommendation largely depends on shifting climate, which triggers a global redistribution of biodiversity, suggesting the inclusion of time as a fourth dimension. Here, we developed a depth-specific prioritization analysis to inform the design of protected areas, further including metrics of climate-driven changes in the ocean. Climate change was captured in this analysis by considering the projected future distribution of >2000 benthic and pelagic species inhabiting the Mediterranean Sea, combined with climatic stability and heterogeneity metrics of the seascape. We identified important areas based on both biological and climatic criteria, where conservation focus should be given in priority when designing a three-dimensional, climate-smart protected area network. We detected spatially concise, conservation priority areas, distributed around the basin, that protected marine areas almost equally across all depth zones. Our approach highlights the importance of deep sea zones as priority areas to meet conservation targets for future marine biodiversity, while suggesting that spatial prioritization schemes, that focus on a static two-dimensional distribution of biodiversity data, might fail to englobe both the vertical properties of species distributions and the fine and larger-scale impacts associated with climate change.

Global assessment of marine and freshwater recreational fish reveals mismatch in climate change vulnerability and conservation effort.

Recreational fisheries contribute substantially to the sociocultural and economic well-being of coastal and riparian regions worldwide, but climate change threatens their sustainability. Fishery managers require information on how climate change will impact key recreational species; however, the absence of a global assessment hinders both directed and widespread conservation efforts. In this study, we present the first global climate change vulnerability assessment of recreationally targeted fish species from marine and freshwater environments (including diadromous fishes). We use climate change projections and data on species' physiological and ecological traits to quantify and map global climate vulnerability and analyze these patterns alongside the indices of socioeconomic value and conservation effort to determine where efforts are sufficient and where they might fall short. We found that over 20% of recreationally targeted fishes are vulnerable to climate change under a high emission scenario. Overall, marine fishes had the highest number of vulnerable species, concentrated in regions with sensitive habitat types (e.g., coral reefs). However, freshwater fishes had higher proportions of species at risk from climate change, with concentrations in northern Europe, Australia, and southern Africa. Mismatches in conservation effort and vulnerability were found within all regions and life-history groups. A key pattern was that current conservation effort focused primarily on marine fishes of high socioeconomic value rather than on the freshwater and diadromous fishes that were predicted to be proportionately more vulnerable. While several marine regions were notably lacking in protection (e.g., Caribbean Sea, Banda Sea), only 19% of vulnerable marine species were without conservation effort. By contrast, 72% of freshwater fishes and 33% of diadromous fishes had no measures in place, despite their high vulnerability and cultural value. The spatial and taxonomic analyses presented here provide guidance for the future conservation and management of recreational fisheries as climate change progresses.

No leading-edge effect in North Atlantic harbor porpoises: Evolutionary and conservation implications.

Understanding species responses to past environmental changes can help forecast how they will cope with ongoing climate changes. Harbor porpoises are widely distributed in the North Atlantic and were deeply impacted by the Pleistocene changes with the split of three subspecies. Despite major impacts of fisheries on natural populations, little is known about population connectivity and dispersal, how they reacted to the Pleistocene changes, and how they will evolve in the future. Here, we used phylogenetics, population genetics, and predictive habitat modeling to investigate population structure and phylogeographic history of the North Atlantic porpoises. A total of 925 porpoises were characterized at 10 microsatellite loci and one quarter of the mitogenome (mtDNA). A highly divergent mtDNA lineage was uncovered in one porpoise off Western Greenland, suggesting that a cryptic group may occur and could belong to a recently discovered mesopelagic ecotype off Greenland. Aside from it and the southern subspecies, spatial genetic variation showed that porpoises from both sides of the North Atlantic form a continuous system belonging to the same subspecies (Phocoena phocoena phocoena). Yet, we identified important departures from random mating and restricted dispersal forming a highly significant isolation by distance (IBD) at both mtDNA and nuclear markers. A ten times stronger IBD at mtDNA compared with nuclear loci supported previous evidence of female philopatry. Together with the lack of spatial trends in genetic diversity, this IBD suggests that migration-drift equilibrium has been reached, erasing any genetic signal of a leading-edge effect that accompanied the predicted recolonization of the northern habitats freed from Pleistocene ice. These results illuminate the processes shaping porpoise population structure and provide a framework for designing conservation strategies and forecasting future population evolution.

Circumpolar phylogeography and demographic history of beluga whales reflect past climatic fluctuations.

Several Arctic marine mammal species are predicted to be negatively impacted by rapid sea ice loss associated with ongoing ocean warming. However, consequences for Arctic whales remain uncertain. To investigate how Arctic whales responded to past climatic fluctuations, we analysed 206 mitochondrial genomes from beluga whales (Delphinapterus leucas) sampled across their circumpolar range, and four nuclear genomes, covering both the Atlantic and the Pacific Arctic region. We found four well-differentiated mitochondrial lineages, which were established before the onset of the last glacial expansion ~110 thousand years ago. Our findings suggested these lineages diverged in allopatry, reflecting isolation of populations during glacial periods when the Arctic sea-shelf was covered by multiyear sea ice. Subsequent population expansion and secondary contact between the Atlantic and Pacific Oceans shaped the current geographic distribution of lineages, and may have facilitated mitochondrial introgression. Our demographic reconstructions based on both mitochondrial and nuclear genomes showed markedly lower population sizes during the Last Glacial Maximum (LGM) compared to the preceding Eemian and current Holocene interglacial periods. Habitat modelling similarly revealed less suitable habitat during the LGM (glacial) than at present (interglacial). Together, our findings suggested the association between climate, population size, and available habitat in belugas. Forecasts for year 2100 showed that beluga habitat will decrease and shift northwards as oceans continue to warm, putatively leading to population declines in some beluga populations. Finally, we identified vulnerable populations which, if extirpated as a consequence of ocean warming, will lead to a substantial decline of species-wide haplotype diversity.

Protecting the global ocean for biodiversity, food and climate.

The ocean contains unique biodiversity, provides valuable food resources and is a major sink for anthropogenic carbon. Marine protected areas (MPAs) are an effective tool for restoring ocean biodiversity and ecosystem services1,2, but at present only 2.7% of the ocean is highly protected3. This low level of ocean protection is due largely to conflicts with fisheries and other extractive uses. To address this issue, here we developed a conservation planning framework to prioritize highly protected MPAs in places that would result in multiple benefits today and in the future. We find that a substantial increase in ocean protection could have triple benefits, by protecting biodiversity, boosting the yield of fisheries and securing marine carbon stocks that are at risk from human activities. Our results show that most coastal nations contain priority areas that can contribute substantially to achieving these three objectives of biodiversity protection, food provision and carbon storage. A globally coordinated effort could be nearly twice as efficient as uncoordinated, national-level conservation planning. Our flexible prioritization framework could help to inform both national marine spatial plans4 and global targets for marine conservation, food security and climate action.

Influence of past climate change on phylogeography and demographic history of narwhals, Monodon monoceros.

The Arctic is warming at an unprecedented rate, with unknown consequences for endemic fauna. However, Earth has experienced severe climatic oscillations in the past, and understanding how species responded to them might provide insight into their resilience to near-future climatic predictions. Little is known about the responses of Arctic marine mammals to past climatic shifts, but narwhals (Monodon monoceros) are considered one of the endemic Arctic species most vulnerable to environmental change. Here, we analyse 121 complete mitochondrial genomes from narwhals sampled across their range and use them in combination with species distribution models to elucidate the influence of past and ongoing climatic shifts on their population structure and demographic history. We find low levels of genetic diversity and limited geographic structuring of genetic clades. We show that narwhals experienced a long-term low effective population size, which increased after the Last Glacial Maximum, when the amount of suitable habitat expanded. Similar post-glacial habitat release has been a key driver of population size expansion of other polar marine predators. Our analyses indicate that habitat availability has been critical to the success of narwhals, raising concerns for their fate in an increasingly warming Arctic.

Postglacial Colonization of Northern Coastal Habitat by Bottlenose Dolphins: A Marine Leading-Edge Expansion?

Oscillations in the Earth's temperature and the subsequent retreating and advancing of ice-sheets around the polar regions are thought to have played an important role in shaping the distribution and genetic structuring of contemporary high-latitude populations. After the Last Glacial Maximum (LGM), retreating of the ice-sheets would have enabled early colonizers to rapidly occupy suitable niches to the exclusion of other conspecifics, thereby reducing genetic diversity at the leading-edge. Bottlenose dolphins (genus Tursiops) form distinct coastal and pelagic ecotypes, with finer-scale genetic structuring observed within each ecotype. We reconstruct the postglacial colonization of the Northeast Atlantic (NEA) by bottlenose dolphins using habitat modeling and phylogenetics. The AquaMaps model hindcasted suitable habitat for the LGM in the Atlantic lower latitude waters and parts of the Mediterranean Sea. The time-calibrated phylogeny, constructed with 86 complete mitochondrial genomes including 30 generated for this study and created using a multispecies coalescent model, suggests that the expansion to the available coastal habitat in the NEA happened via founder events starting ~15 000 years ago (95% highest posterior density interval: 4 900-26 400). The founders of the 2 distinct coastal NEA populations comprised as few as 2 maternal lineages that originated from the pelagic population. The low effective population size and genetic diversity estimated for the shared ancestral coastal population subsequent to divergence from the pelagic source population are consistent with leading-edge expansion. These findings highlight the legacy of the Late Pleistocene glacial cycles on the genetic structuring and diversity of contemporary populations.

Global assessment of marine biodiversity potentially threatened by offshore hydrocarbon activities.

Increasing global energy demands have led to the ongoing intensification of hydrocarbon extraction from marine areas. Hydrocarbon extractive activities pose threats to native marine biodiversity, such as noise, light, and chemical pollution, physical changes to the sea floor, invasive species, and greenhouse gas emissions. Here, we assessed at a global scale the spatial overlap between offshore hydrocarbon activities and marine biodiversity (>25,000 species, nine major ecosystems, and marine protected areas), and quantify the changes over time. We discovered that two-thirds of global offshore hydrocarbon activities occur in areas within the top 10% for species richness, range rarity, and proportional range rarity values globally. Thus, while hydrocarbon activities are undertaken in less than one percent of the ocean's area, they overlap with approximately 85% of all assessed species. Of conservation concern, 4% of species with the largest proportion of their range overlapping hydrocarbon activities are range restricted, potentially increasing their vulnerability to localized threats such as oil spills. While hydrocarbon activities have extended to greater depths since the mid-1990s, we found that the largest overlap is with coastal ecosystems, particularly estuaries, saltmarshes and mangroves. Furthermore, in most countries where offshore hydrocarbon exploration licensing blocks have been delineated, they do not overlap with marine protected areas (MPAs). Although this is positive in principle, many countries have far more licensing block areas than protected areas, and in some instances, MPA coverage is minimal. These findings suggest the need for marine spatial prioritization to help limit future spatial overlap between marine conservation priorities and hydrocarbon activities. Such prioritization can be informed by the spatial and quantitative baseline information provided here. In increasingly shared seascapes, prioritizing management actions that set both conservation and development targets could help minimize further declines of biodiversity and environmental changes at a global scale.

Metabolic asymmetry and the global diversity of marine predators.

Species richness of marine mammals and birds is highest in cold, temperate seas-a conspicuous exception to the general latitudinal gradient of decreasing diversity from the tropics to the poles. We compiled a comprehensive dataset for 998 species of sharks, fish, reptiles, mammals, and birds to identify and quantify inverse latitudinal gradients in diversity, and derived a theory to explain these patterns. We found that richness, phylogenetic diversity, and abundance of marine predators diverge systematically with thermoregulatory strategy and water temperature, reflecting metabolic differences between endotherms and ectotherms that drive trophic and competitive interactions. Spatial patterns of foraging support theoretical predictions, with total prey consumption by mammals increasing by a factor of 80 from the equator to the poles after controlling for productivity.

An inverse latitudinal gradient in speciation rate for marine fishes.

Far more species of organisms are found in the tropics than in temperate and polar regions, but the evolutionary and ecological causes of this pattern remain controversial1,2. Tropical marine fish communities are much more diverse than cold-water fish communities found at higher latitudes3,4, and several explanations for this latitudinal diversity gradient propose that warm reef environments serve as evolutionary 'hotspots' for species formation5-8. Here we test the relationship between latitude, species richness and speciation rate across marine fishes. We assembled a time-calibrated phylogeny of all ray-finned fishes (31,526 tips, of which 11,638 had genetic data) and used this framework to describe the spatial dynamics of speciation in the marine realm. We show that the fastest rates of speciation occur in species-poor regions outside the tropics, and that high-latitude fish lineages form new species at much faster rates than their tropical counterparts. High rates of speciation occur in geographical regions that are characterized by low surface temperatures and high endemism. Our results reject a broad class of mechanisms under which the tropics serve as an evolutionary cradle for marine fish diversity and raise new questions about why the coldest oceans on Earth are present-day hotspots of species formation.

Demography or selection on linked cultural traits or genes? Investigating the driver of low mtDNA diversity in the sperm whale using complementary mitochondrial and nuclear genome analyses.

Mitochondrial DNA has been heavily utilized in phylogeography studies for several decades. However, underlying patterns of demography and phylogeography may be misrepresented due to coalescence stochasticity, selection, variation in mutation rates and cultural hitchhiking (linkage of genetic variation to culturally-transmitted traits affecting fitness). Cultural hitchhiking has been suggested as an explanation for low genetic diversity in species with strong social structures, counteracting even high mobility, abundance and limited barriers to dispersal. One such species is the sperm whale, which shows very limited phylogeographic structure and low mtDNA diversity despite a worldwide distribution and large population. Here, we use analyses of 175 globally distributed mitogenomes and three nuclear genomes to evaluate hypotheses of a population bottleneck/expansion vs. a selective sweep due to cultural hitchhiking or selection on mtDNA as the mechanism contributing to low worldwide mitochondrial diversity in sperm whales. In contrast to mtDNA control region (CR) data, mitogenome haplotypes are largely ocean-specific, with only one of 80 shared between the Atlantic and Pacific. Demographic analyses of nuclear genomes suggest low mtDNA diversity is consistent with a global reduction in population size that ended approximately 125,000 years ago, correlated with the Eemian interglacial. Phylogeographic analysis suggests that extant sperm whales descend from maternal lineages endemic to the Pacific during the period of reduced abundance and have subsequently colonized the Atlantic several times. Results highlight the apparent impact of past climate change, and suggest selection and hitchhiking are not the sole processes responsible for low mtDNA diversity in this highly social species.

Assessing cetacean surveys throughout the Mediterranean Sea: a gap analysis in environmental space.

Heterogeneous data collection in the marine environment has led to large gaps in our knowledge of marine species distributions. To fill these gaps, models calibrated on existing data may be used to predict species distributions in unsampled areas, given that available data are sufficiently representative. Our objective was to evaluate the feasibility of mapping cetacean densities across the entire Mediterranean Sea using models calibrated on available survey data and various environmental covariates. We aggregated 302,481 km of line transect survey effort conducted in the Mediterranean Sea within the past 20 years by many organisations. Survey coverage was highly heterogeneous geographically and seasonally: large data gaps were present in the eastern and southern Mediterranean and in non-summer months. We mapped the extent of interpolation versus extrapolation and the proportion of data nearby in environmental space when models calibrated on existing survey data were used for prediction across the entire Mediterranean Sea. Using model predictions to map cetacean densities in the eastern and southern Mediterranean, characterised by warmer, less productive waters, and more intense eddy activity, would lead to potentially unreliable extrapolations. We stress the need for systematic surveys of cetaceans in these environmentally unique Mediterranean waters, particularly in non-summer months.

Aligning marine species range data to better serve science and conservation.

Species distribution data provide the foundation for a wide range of ecological research studies and conservation management decisions. Two major efforts to provide marine species distributions at a global scale are the International Union for Conservation of Nature (IUCN), which provides expert-generated range maps that outline the complete extent of a species' distribution; and AquaMaps, which provides model-generated species distribution maps that predict areas occupied by the species. Together these databases represent 24,586 species (93.1% within AquaMaps, 16.4% within IUCN), with only 2,330 shared species. Differences in intent and methodology can result in very different predictions of species distributions, which bear important implications for scientists and decision makers who rely upon these datasets when conducting research or informing conservation policy and management actions. Comparing distributions for the small subset of species with maps in both datasets, we found that AquaMaps and IUCN range maps show strong agreement for many well-studied species, but our analysis highlights several key examples in which introduced errors drive differences in predicted species ranges. In particular, we find that IUCN maps greatly overpredict coral presence into unsuitably deep waters, and we show that some AquaMaps computer-generated default maps (only 5.7% of which have been reviewed by experts) can produce odd discontinuities at the extremes of a species' predicted range. We illustrate the scientific and management implications of these tradeoffs by repeating a global analysis of gaps in coverage of marine protected areas, and find significantly different results depending on how the two datasets are used. By highlighting tradeoffs between the two datasets, we hope to encourage increased collaboration between taxa experts and large scale species distribution modeling efforts to further improve these foundational datasets, helping to better inform science and policy recommendations around understanding, managing, and protecting marine biodiversity.