Are Mediterranean marine threatened species at high risk by climate change?

Rapid anthropogenic climate change is driving threatened biodiversity one step closer to extinction. Effects on native biodiversity are determined by an interplay between species' exposure to climate change and their specific ecological and life-history characteristics that render them even more susceptible. Impacts on biodiversity have already been reported, however, a systematic risk evaluation of threatened marine populations is lacking. Here, we employ a trait-based approach to assess the risk of 90 threatened marine Mediterranean species to climate change, combining species' exposure to increased sea temperature and intrinsic vulnerability. One-quarter of the threatened marine biodiversity of the Mediterranean Sea is predicted to be under elevated levels of climate risk, with various traits identified as key vulnerability traits. High-risk taxa including sea turtles, marine mammals, Anthozoa and Chondrichthyes are highlighted. Climate risk, vulnerability and exposure hotspots are distributed along the Western Mediterranean, Alboran, Aegean, and Adriatic Seas. At each Mediterranean marine ecoregion, 21%-31% of their threatened species have high climate risk. All Mediterranean marine protected areas host threatened species with high risk to climate change, with 90% having a minimum of 4 up to 19 species of high climate risk, making the objective of a climate-smart conservation strategy a crucial task for immediate planning and action. Our findings aspire to offer new insights for systematic, spatially strategic planning and prioritization of vulnerable marine life in the face of accelerating climate change.

Priorities for Mediterranean marine turtle conservation and management in the face of climate change.

As climate-related impacts threaten marine biodiversity globally, it is important to adjust conservation efforts to mitigate the effects of climate change. Translating scientific knowledge into practical management, however, is often complicated due to resource, economic and policy constraints, generating a knowledge-action gap. To develop potential solutions for marine turtle conservation, we explored the perceptions of key actors across 18 countries in the Mediterranean. These actors evaluated their perceived relative importance of 19 adaptation and mitigation measures that could safeguard marine turtles from climate change. Of importance, despite differences in expertise, experience and focal country, the perceptions of researchers and management practitioners largely converged with respect to prioritizing adaptation and mitigation measures. Climate change was considered to have the greatest impacts on offspring sex ratios and suitable nesting sites. The most viable adaptation/mitigation measures were considered to be reducing other pressures that act in parallel to climate change. Ecological effectiveness represented a key determinant for implementing proposed measures, followed by practical applicability, financial cost, and societal cost. This convergence in opinions across actors likely reflects long-standing initiatives in the Mediterranean region towards supporting knowledge exchange in marine turtle conservation. Our results provide important guidance on how to prioritize measures that incorporate climate change in decision-making processes related to the current and future management and protection of marine turtles at the ocean-basin scale, and could be used to guide decisions in other regions globally. Importantly, this study demonstrates a successful example of how interactive processes can be used to fill the knowledge-action gap between research and management.

Spatial heterogeneity and temporal stability characterize future climatic refugia in Mediterranean Europe.

Climate plays a major role in shaping biodiversity patterns over time and space, with ongoing changes leading to the reorganization of ecosystems, which challenges conservation initiatives. Identifying areas that could serve as possible climate change refugia for future biodiversity is, thus, critical for both conservation and management. Here, we identify potential future climatic refugia within the Euro-Mediterranean biome, which is a global biodiversity hotspot, while accounting for multiple emission climate change projections over the next 50 years. We developed two metrics of climatic variability: temporal stability and spatial heterogeneity. We then used a systematic conservation planning approach to identify climate-based priority areas. While we used a climate-based, species-neutral methodology, we deliberately implemented low climatic velocity thresholds, so that the identified climatic refugia would even be compatible with the needs of species with low dispersal capacity, such as plants. Our projections showed that future climatic refugia would be more frequently observed in mid-altitudes, for gradients with steep elevations, and mainly in the eastern part of the Euro-Mediterranean biome, with possible conflicts with existing land uses and future conservation implications. Climatic, land use, and topography results indicated that only a limited number of refugia would be hosted by high elevation habitats (>1500 m), raising possible concerns about the biodiversity of Mediterranean mountain regions. Our analyses show that the current network of protected areas captures future climatic refugia disproportionally, despite their importance for safeguarding present and future biodiversity in the Mediterranean. Key climatic refugia could limit the impacts of future climate change on biodiversity in mid-altitude and mountainous regions, and should be included in management guidelines for a climate-ready conservation design in the Mediterranean biome.

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.

Making spatial-temporal marine ecosystem modelling better - A perspective.

Marine Ecosystem Models (MEMs) provide a deeper understanding of marine ecosystem dynamics. The United Nations Decade of Ocean Science for Sustainable Development has highlighted the need to deploy these complex mechanistic spatial-temporal models to engage policy makers and society into dialogues towards sustainably managed oceans. From our shared perspective, MEMs remain underutilized because they still lack formal validation, calibration, and uncertainty quantifications that undermines their credibility and uptake in policy arenas. We explore why these shortcomings exist and how to enable the global modelling community to increase MEMs' usefulness. We identify a clear gap between proposed solutions to assess model skills, uncertainty, and confidence and their actual systematic deployment. We attribute this gap to an underlying factor that the ecosystem modelling literature largely ignores: technical issues. We conclude by proposing a conceptual solution that is cost-effective, scalable and simple, because complex spatial-temporal marine ecosystem modelling is already complicated enough.

A fast-moving target: achieving marine conservation goals under shifting climate and policies.

In the Anthropocene, marine ecosystems are rapidly shifting to new ecological states. Achieving effective conservation of marine biodiversity has become a fast-moving target because of both global climate change and continuous shifts in marine policies. How prepared are we to deal with this crisis? We examined EU Member States Programs of Measures designed for the implementation of EU marine environmental policies, as well as recent European Marine Spatial Plans, and discovered that climate change is rarely considered operationally. Further, our analysis revealed that monitoring programs in marine protected areas are often insufficient to clearly distinguish between impacts of local and global stressors. Finally, we suggest that while the novel global Blue Growth approach may jeopardize previous marine conservation efforts, it can also provide new conservation opportunities. Adaptive management is the way forward (e.g., preserving ecosystem functions in climate change hotspots, and identifying and targeting climate refugia areas for protection) using Marine Spatial Planning as a framework for action, especially given the push for Blue Growth.

A Review of Patterns of Multiple Paternity Across Sea Turtle Rookeries.

Why females would mate with multiple partners and have multiple fathers for clutches or litters is a long-standing enigma. There is a broad dichotomy in hypotheses ranging from polyandry having benefits to simply being an unavoidable consequence of a high incidence of male-female encounters. If females simply give in to mating when it is too costly to avoid being harassed by males (convenience polyandry), then there should be a higher rate of mating as density increases. However, if females actively seek males because they benefit from multiple mating, then mating frequency, and consequently the incidence of multiple paternity of clutches, should be high throughout. To explore these competing explanations, here we review the incidence of multiple paternity for sea turtles nesting around the World. Across 30 rookeries, including all 7 species of sea turtle, the incidence of multiple paternity was only weakly linked to rookery size (r2=0.14). However, using high resolution at-sea GPS tracking we show that the specifics of movement patterns play a key role in driving packing density and hence the likely rate of male-female encounters. When individuals use the same focal areas, packing density could be 100× greater than when assuming individuals move independently. Once the extent of adult movements in the breeding season was considered so that movements and abundance could be combined to produce a measure of density, then across rookeries we found a very tight relationship (r2=0.96) between packing density and the incidence of multiple paternity. These findings suggest that multiple paternity in sea turtles may have no benefit, but is simply a consequence of the incidence of male-female encounters.

Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination.

For species with temperature-dependent sex determination (TSD) there is the fear that rising temperatures may lead to single-sex populations and population extinction. We show that for sea turtles, a major group exhibiting TSD, these concerns are currently unfounded but may become important under extreme climate warming scenarios. We show how highly female-biased sex ratios in developing eggs translate into much more balanced operational sex ratios so that adult male numbers in populations around the world are unlikely to be limiting. Rather than reducing population viability, female-biased offspring sex ratios may, to some extent, help population growth by increasing the number of breeding females and hence egg production. For rookeries across the world (n = 75 sites for seven species), we show that extreme female-biased hatchling sex ratios do not compromise population size and are the norm, with a tendency for populations to maximize the number of female hatchlings. Only at extremely high incubation temperature does high mortality within developing clutches threaten sea turtles. Our work shows how TSD itself is a robust strategy up to a point, but eventually high mortality and female-only hatchling production will cause extinction if incubation conditions warm considerably in the future.

Landscape structure and diseases profile: associating land use type composition with disease distribution.

Human health and well-being presuppose environmental quality. Several studies have documented the indicative role of land use types in environmental quality. However, the exact role of land use composition on disease distribution has remained scientifically vague. We assessed the congruence of diseases' distribution with land use composition, focusing on high environmental quality areas, defined as tranquil areas with view to indicating places offering well-being. Landscape composition is linked to the presence of diseases across 51 prefectures of Greece. Agricultural and natural land use types proved to be the main drivers of disease distribution. Tranquility demonstrated a strong negative correlation with population density, thus could be considered as a quantitative spatial index of life-quality. We concluded that the landscape context affects the dominance of diseases' patterns. Special emphasis should be put on the role of tranquil areas in human health and the relative environmental health policies.

Thermal vulnerability of sea turtle foraging grounds around the globe.

Anticipating and mitigating the impacts of climate change on biodiversity requires a comprehensive understanding on key habitats utilized by species. Yet, such information for high mobile marine megafauna species remains limited. Here, we compile a global database comprising published satellite tracking data (n = 1035 individuals) to spatially delineate foraging grounds for seven sea turtle species and assess their thermal stability. We identified 133 foraging areas distributed around the globe, of which only 2% of the total surface is enclosed within an existing protected area. One-third of the total coverage of foraging hotspots is situated in high seas, where conservation focus is often neglected. Our analyses revealed that more than two-thirds of these vital marine habitats will experience new sea surface temperature (SST) conditions by 2100, exposing sea turtles to potential thermal risks. Our findings underline the importance of global ocean conservation efforts, which can meet climate challenges even in remote environments.

Reprint: A Review of Patterns of Multiple Paternity Across Sea Turtle Rookeries.

Why females would mate with multiple partners and have multiple fathers for clutches or litters is a long-standing enigma. There is a broad dichotomy in hypotheses ranging from polyandry having benefits to simply being an unavoidable consequence of a high incidence of male-female encounters. If females simply give in to mating when it is too costly to avoid being harassed by males (convenience polyandry), then there should be a higher rate of mating as density increases. However, if females actively seek males because they benefit from multiple mating, then mating frequency, and consequently the incidence of multiple paternity of clutches, should be high throughout. To explore these competing explanations, here we review the incidence of multiple paternity for sea turtles nesting around the World. Across 30 rookeries, including all 7 species of sea turtle, the incidence of multiple paternity was only weakly linked to rookery size (r2=0.14). However, using high resolution at-sea GPS tracking we show that the specifics of movement patterns play a key role in driving packing density and hence the likely rate of male-female encounters. When individuals use the same focal areas, packing density could be 100× greater than when assuming individuals move independently. Once the extent of adult movements in the breeding season was considered so that movements and abundance could be combined to produce a measure of density, then across rookeries we found a very tight relationship (r2=0.96) between packing density and the incidence of multiple paternity. These findings suggest that multiple paternity in sea turtles may have no benefit, but is simply a consequence of the incidence of male-female encounters.

A pulse check for trends in sea turtle numbers across the globe.

Population declines of vertebrates are common, but rebuilding marine life may be possible. We assessed trends in sea turtle numbers globally, building 61 time series of abundance extending beyond 2015, representing monitoring in >1200 years. Increases were widespread with significant upward trends, no significant change, and significant downward trends in 28, 28, and 5 time series, respectively. For example, annual nest numbers increased between 1980 and 2018 from around 4,000 to 16,000 for green turtles at Aldabra (Seychelles, Indian Ocean) and between 2008 and 2020 from around 500 to 35,000 for loggerhead turtles in Sal (Cape Verde, north Atlantic). However, conservation concerns remain. Major populations may experience declines, such as loggerhead turtles in Oman, while previous upward trends can be reversed, as with green turtles nesting at Tortuguero (Costa Rica, Caribbean). Further, decreases in abundance were evident in several leatherback turtle time series. These concerns show there is no room for complacency for sea turtle conservation.

Phenological response of sea turtles to environmental variation across a species' northern range.

Variations in environmental parameters (e.g. temperature) that form part of global climate change have been associated with shifts in the timing of seasonal events for a broad range of organisms. Most studies evaluating such phenological shifts of individual taxa have focused on a limited number of locations, making it difficult to assess how such shifts vary regionally across a species range. Here, by using 1445 records of the date of first nesting for loggerhead sea turtles (Caretta caretta) at different breeding sites, on different continents and in different years across a broad latitudinal range (25-39° 'N), we demonstrate that the gradient of the relationship between temperature and the date of first breeding is steeper at higher latitudes, i.e. the phenological responses to temperature appear strongest at the poleward range limit. These findings support the hypothesis that biological changes in response to climate change will be most acute at the poleward range limits and are in accordance with the predictions of MacArthur's hypothesis that poleward range limit for species range is environmentally limited. Our findings imply that the poleward populations of loggerheads are more sensitive to climate variations and thus they might display the impacts of climate change sooner and more prominently.

Human activities in Natura 2000 sites: a highly diversified conservation network.

The Natura 2000 network was established across the European Union's (EU) Member States with the aim to conserve biodiversity, while ensuring the sustainability of human activities. However, to what kind and to what extent Natura 2000 sites are subject to human activities and how this varies across Member States remains unspecified. Here, we analyzed 111,269 human activity records from 14,727 protected sites in 20 Member States. The frequency of occurrence of activities differs among countries, with more than 86 % of all sites being subjected to agriculture or forestry. Activities like hunting, fishing, urbanization, transportation, and tourism are more frequently recorded in south European sites than in northern or eastern ones. The observed variations indicate that Natura 2000 networks are highly heterogeneous among EU Member States. Our analysis highlights the importance of agriculture in European landscapes and indicates possible targets for policy interventions at national, European, or "sub-European" level. The strong human presence in the Natura 2000 network throughout Member States, shows that conservation initiatives could succeed only by combining social and ecological sustainability and by ensuring the integration of policies affecting biodiversity.

Novel climates in European river sub-basins pose a challenge for the persistence of freshwater fish.

Understanding how climate change would affect biota inhabiting sensitive and highly valuable ecosystems, spanning broad regions, is essential to anticipate implications for biodiversity and humans, and to identify management and mitigation measures. Traditionally, assessments to evaluate climatic risks over broad regions and for many species implement models that allow the projection of a climate-driven redistribution of biodiversity. Still, the wealth and quality of the background information (e.g., species presence data) constrain the accuracy and representativeness of such frameworks. As an alternative, here, we developed a twofold approach to assess the vulnerability of 86 European freshwater fish. We accounted for shifts in a multidimensional climatic space of broader hydrological units that host freshwater bodies in Europe. We then linked metrics of their climatic stability with groups of species, which were generated from six intrinsic traits that shape species adaptive capacity to climate change. Our results demonstrated that the climate of all (n = 538) river sub-basins hosted in the European Union territory would change by 2100, with more than 10% of them being projected to gain completely novel climates. Sub-basins predicted to lose more than 90% of their current climatic space were mainly identified in the area around the Baltic Sea, but also in Mediterranean regions (i.e., Iberian Peninsula). Important numbers of fish species with life history strategies that are considered susceptible to climate change were identified in sub-basins that were predicted to completely lose their current climatic conditions. Clearly, the climate of valuable freshwater ecosystems is changing, affecting species and their communities in varying ways. The risk is high, and is not limited to specific regions; thus, new effective strategies and measures are needed to conserve freshwater fish and their habitats across Europe.

Functional extinction of dugongs in China.

Dugongs (Dugong dugon) experienced a serious population decline in China during the twentieth century, and their regional status is poorly understood. To determine their current distribution and status, we conducted a large-scale interview survey of marine resource users across four Chinese provinces and reviewed all available historical data covering the past distribution of dugongs in Chinese waters. Only 5% of 788 respondents reported past dugong sightings, with a mean last-sighting date of 23 years earlier, and only three respondents reported sightings from within the past 5 years. Historical records of dugongs peak around 1960 and then decrease rapidly from 1975 onwards; no records are documented after 2008, with no verified field observations after 2000. Based on these findings, we are forced to conclude that dugongs have experienced rapid population collapse during recent decades and are now functionally extinct in China. Our study provides evidence of a new regional loss of a charismatic marine megafaunal species, and the first reported functional extinction of a large vertebrate in Chinese marine waters. This rapid documented population collapse also serves as a sobering reminder that extinctions can occur before effective conservation actions are developed.

A catastrophic change in a european protected wetland: From harmful phytoplankton blooms to fish and bird kill.

Understanding the processes that underlay an ecological disaster represents a major scientific challenge. Here, we investigated phytoplankton and zooplankton community changes before and during a fauna mass kill in a European protected wetland. Evidence on gradual development and collapse of harmful phytoplankton blooms, allowed us to delineate the biotic and abiotic interactions that led to this ecological disaster. Before the mass fauna kill, mixed blooms of known harmful cyanobacteria and the killer alga Prymnesium parvum altered biomass flow and minimized zooplankton resource use efficiency. These blooms collapsed under high nutrient concentrations and inhibitory ammonia levels, with low phytoplankton biomass leading to a dramatic drop in photosynthetic oxygenation and a shift to a heterotrophic ecosystem phase. Along with the phytoplankton collapse, extremely high numbers of red planktonic crustaceans-Daphnia magna, visible through satellite images, indicated low oxygen conditions as well as a decrease or absence of fish predation pressure. Our findings provide clear evidence that the mass episode of fish and birds kill resulted through severe changes in phytoplankton and zooplankton dynamics, and the alternation on key abiotic conditions. Our study highlights that plankton-related ecosystem functions mirror the accumulated heavy anthropogenic impacts on freshwaters and could reflect a failure in conservation and restoration measures.

Is the current Mediterranean network of marine protected areas resilient to climate change?

Rising ocean temperature impacts the functionality and structure of ecosystems, further triggering the redistribution of biodiversity. Still, the magnitude and anticipated impacts of ocean warming are not expected to be uniform across marine space. Here, we developed a two-fold index-based approach to provide an integrated climatic vulnerability assessment of the marine surfaces which are enclosed within protected areas in the Mediterranean Sea. We first built a climatic stability index, based on metrics of analog-based velocity of climate change over a 120-year period (1950-2069), to assess patterns of climate dynamics within the marine protected surfaces. To provide a vulnerability ranking of protected surfaces under climate change, we combined this climate-related index with an index of community stability, reflecting the projected distribution shifts of 71 species of high conservation value. Our analyses revealed a highly heterogeneous and dynamic climatic space, with increasing but spatially inconsistent patterns of climate change velocities over successive 30-year periods. We found that about 62% of the protected marine surface might be subjected to low/very low climatic stability. About 70% of the protected waters were also found to be of limited community stability. Thus, protected surfaces across the Mediterranean basin were characterized by high vulnerability under changing climatic conditions, while only 5.7% of them exhibited high and very high stability based on both indices. Our findings suggest that combining information on climate change dynamics and biotic stability could offer spatially explicit insights which cannot be obtained based simply on the ecological dimensions of conservation planning.

A review of the combined effects of climate change and other local human stressors on the marine environment.

Climate change (CC) is a key, global driver of change of marine ecosystems. At local and regional scales, other local human stressors (LS) can interact with CC and modify its effects on marine ecosystems. Understanding the response of the marine environment to the combined effects of CC and LS is crucial to inform marine ecosystem-based management and planning, yet our knowledge of the potential effects of such interactions is fragmented. At a global scale, we explored how cumulative effect assessments (CEAs) have addressed CC in the marine realm and discuss progress and shortcomings of current approaches. For this we conducted a systematic review on how CEAs investigated at different levels of biological organization ecological responses, functional aspects, and the combined effect of CC and HS. Globally, the effects of 52 LS and of 27 CC-related stressors on the marine environment have been studied in combination, such as industrial fisheries with change in temperature, or sea level rise with artisanal fisheries, marine litter, change in sediment load and introduced alien species. CC generally intensified the effects of LS at species level. At trophic groups and ecosystem levels, the effects of CC either intensified or mitigated the effects of other HS depending on the trophic groups or the environmental conditions involved, thus suggesting that the combined effects of CC and LS are context-dependent and vary among and within ecosystems. Our results highlight that large-scale assessments on the spatial interaction and combined effects of CC and LS remain limited. More importantly, our results strengthen the urgent need of CEAs to capture local-scale effects of stressors that can exacerbate climate-induced changes. Ultimately, this will allow identifying management measures that aid counteracting CC effects at relevant scales.