Cross-basin and cross-taxa patterns of marine community tropicalization and deborealization in warming European seas.

Ocean warming and acidification, decreases in dissolved oxygen concentrations, and changes in primary production are causing an unprecedented global redistribution of marine life. The identification of underlying ecological processes underpinning marine species turnover, particularly the prevalence of increases of warm-water species or declines of cold-water species, has been recently debated in the context of ocean warming. Here, we track changes in the mean thermal affinity of marine communities across European seas by calculating the Community Temperature Index for 65 biodiversity time series collected over four decades and containing 1,817 species from different communities (zooplankton, coastal benthos, pelagic and demersal invertebrates and fish). We show that most communities and sites have clearly responded to ongoing ocean warming via abundance increases of warm-water species (tropicalization, 54%) and decreases of cold-water species (deborealization, 18%). Tropicalization dominated Atlantic sites compared to semi-enclosed basins such as the Mediterranean and Baltic Seas, probably due to physical barrier constraints to connectivity and species colonization. Semi-enclosed basins appeared to be particularly vulnerable to ocean warming, experiencing the fastest rates of warming and biodiversity loss through deborealization.

Northeast Atlantic elasmobranch community on the move: Functional reorganization in response to climate change.

While spatial distribution shifts have been documented in many marine fishes under global change, the responses of elasmobranchs have rarely been studied, which may have led to an underestimation of their potential additional threats. Given their irreplaceable role in ecosystems and their high extinction risk, we used a 24-year time series (1997-2020) of scientific bottom trawl surveys to examine the effects of climate change on the spatial distribution of nine elasmobranch species within Northeast Atlantic waters. Using a hierarchical modeling of species communities, belonging to the joint species distribution models, we found that suitable habitats for four species increased on average by a factor of 1.6 and, for six species, shifted north-eastwards and/or to deeper waters over the past two decades. By integrating species traits, we showed changes in habitat suitability led to changes in the elasmobranchs trait composition. Moreover, communities shifted to deeper waters and their mean trophic level decreased. We also note an increase in the mean community size at maturity concurrent with a decrease in fecundity. Because skates and sharks are functionally unique and dangerously vulnerable to both climate change and fishing, we advocate for urgent considerations of species traits in management measures. Their use would make it better to identify species whose loss could have irreversible impacts in face of the myriad of anthropogenic threats.

Marine heatwaves are not a dominant driver of change in demersal fishes.

Marine heatwaves have been linked to negative ecological effects in recent decades1,2. If marine heatwaves regularly induce community reorganization and biomass collapses in fishes, the consequences could be catastrophic for ecosystems, fisheries and human communities3,4. However, the extent to which marine heatwaves have negative impacts on fish biomass or community composition, or even whether their effects can be distinguished from natural and sampling variability, remains unclear. We investigated the effects of 248 sea-bottom heatwaves from 1993 to 2019 on marine fishes by analysing 82,322 hauls (samples) from long-term scientific surveys of continental shelf ecosystems in North America and Europe spanning the subtropics to the Arctic. Here we show that the effects of marine heatwaves on fish biomass were often minimal and could not be distinguished from natural and sampling variability. Furthermore, marine heatwaves were not consistently associated with tropicalization (gain of warm-affiliated species) or deborealization (loss of cold-affiliated species) in these ecosystems. Although steep declines in biomass occasionally occurred after marine heatwaves, these were the exception, not the rule. Against the highly variable backdrop of ocean ecosystems, marine heatwaves have not driven biomass change or community turnover in fish communities that support many of the world's largest and most productive fisheries.

The ecological causes of functional distinctiveness in communities.

Recent work has shown that evaluating functional trait distinctiveness, the average trait distance of a species to other species in a community offers promising insights into biodiversity dynamics and ecosystem functioning. However, the ecological mechanisms underlying the emergence and persistence of functionally distinct species are poorly understood. Here, we address the issue by considering a heterogeneous fitness landscape whereby functional dimensions encompass peaks representing trait combinations yielding positive population growth rates in a community. We identify four ecological cases contributing to the emergence and persistence of functionally distinct species. First, environmental heterogeneity or alternative phenotypic designs can drive positive population growth of functionally distinct species. Second, sink populations with negative population growth can deviate from local fitness peaks and be functionally distinct. Third, species found at the margin of the fitness landscape can persist but be functionally distinct. Fourth, biotic interactions (positive or negative) can dynamically alter the fitness landscape. We offer examples of these four cases and guidelines to distinguish between them. In addition to these deterministic processes, we explore how stochastic dispersal limitation can yield functional distinctiveness. Our framework offers a novel perspective on the relationship between fitness landscape heterogeneity and the functional composition of ecological assemblages.

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.

Disentangling tropicalization and deborealization in marine ecosystems under climate change.

As climate change accelerates, species are shifting poleward and subtropical and tropical species are colonizing temperate environments.1-3 A popular approach for characterizing such responses is the community temperature index (CTI), which tracks the mean thermal affinity of a community. Studies in marine,4 freshwater,5 and terrestrial6 ecosystems have documented increasing CTI under global warming. However, most studies have only linked increasing CTI to increases in warm-affinity species. Here, using long-term monitoring of marine fishes across the Northern Hemisphere, we decomposed CTI changes into four underlying processes-tropicalization (increasing warm-affinity), deborealization (decreasing cold-affinity), borealization (increasing cold-affinity), and detropicalization (decreasing warm-affinity)-for which we examined spatial variability and drivers. CTI closely tracked changes in sea surface temperature, increasing in 72% of locations. However, 31% of these increases were primarily due to decreases in cold-affinity species, i.e., deborealization. Thus, increases in warm-affinity species were prevalent, but not ubiquitous. Tropicalization was stronger in areas that were initially warmer, experienced greater warming, or were deeper, while deborealization was stronger in areas that were closer to human population centers or that had higher community thermal diversity. When CTI (and temperature) increased, species that decreased were more likely to be living closer to their upper thermal limits or to be commercially fished. Additionally, warm-affinity species that increased had smaller body sizes than those that decreased. Our results show that CTI changes arise from a variety of underlying community responses that are linked to environmental conditions, human impacts, community structure, and species characteristics.

The dimensionality and structure of species trait spaces.

Trait-based ecology aims to understand the processes that generate the overarching diversity of organismal traits and their influence on ecosystem functioning. Achieving this goal requires simplifying this complexity in synthetic axes defining a trait space and to cluster species based on their traits while identifying those with unique combinations of traits. However, so far, we know little about the dimensionality, the robustness to trait omission and the structure of these trait spaces. Here, we propose a unified framework and a synthesis across 30 trait datasets representing a broad variety of taxa, ecosystems and spatial scales to show that a common trade-off between trait space quality and operationality appears between three and six dimensions. The robustness to trait omission is generally low but highly variable among datasets. We also highlight invariant scaling relationships, whatever organismal complexity, between the number of clusters, the number of species in the dominant cluster and the number of unique species with total species richness. When species richness increases, the number of unique species saturates, whereas species tend to disproportionately pack in the richest cluster. Based on these results, we propose some rules of thumb to build species trait spaces and estimate subsequent functional diversity indices.

Trait similarity in reef fish faunas across the world's oceans.

Species' traits, rather than taxonomic identities, determine community assembly and ecosystem functioning, yet biogeographic patterns have been far less studied for traits. While both environmental conditions and evolutionary history shape trait biogeography, their relative contributions are largely unknown for most organisms. Here, we explore the global biogeography of reef fish traits for 2,786 species from 89 ecoregions spanning eight marine realms with contrasting environmental conditions and evolutionary histories. Across realms, we found a common structure in the distribution of species traits despite a 10-fold gradient in species richness, with a defined "backbone" of 21 trait combinations shared by all realms globally, both temperate and tropical. Across ecoregions, assemblages under similar environmental conditions had similar trait compositions despite hosting drastically different species pools from separate evolutionary lineages. Thus, despite being separated by thousands of kilometers and millions of years of evolution, similar environments host similar trait compositions in reef fish assemblages worldwide. Our findings suggest that similar trait-based management strategies can be applied among regions with distinct species pools, potentially improving conservation outcomes across diverse jurisdictions.

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.

Rebound in functional distinctiveness following warming and reduced fishing in the North Sea.

Functionally distinct species (i.e. species with unique trait combinations in the community) can support important ecological roles and contribute disproportionately to ecosystem functioning. Yet, how functionally distinct species have responded to recent climate change and human exploitation has been widely overlooked. Here, using ecological traits and long-term fish data in the North Sea, we identified functionally distinct and functionally common species, and evaluated their spatial and temporal dynamics in relation to environmental variables and fishing pressure. Functionally distinct species were characterized by late sexual maturity, few, large offspring, and high parental care, many being sharks and skates that play critical roles in structuring food webs. Both functionally distinct and functionally common species increased in abundance as ocean temperatures warmed and fishing pressure decreased over the last three decades; however, functionally distinct species increased throughout the North Sea, but primarily in southern North Sea where fishing was historically most intense, indicating a rebound following fleet decommissioning and reduced harvesting. Yet, some of the most functionally distinct species are currently listed as threatened by the IUCN and considered highly vulnerable to fishing pressure. Alarmingly these species have not rebounded. This work highlights the relevance and potential of integrating functional distinctiveness into ecosystem management and conservation prioritization.

Are we ready to track climate-driven shifts in marine species across international boundaries? - A global survey of scientific bottom trawl data.

Marine biota are redistributing at a rapid pace in response to climate change and shifting seascapes. While changes in fish populations and community structure threaten the sustainability of fisheries, our capacity to adapt by tracking and projecting marine species remains a challenge due to data discontinuities in biological observations, lack of data availability, and mismatch between data and real species distributions. To assess the extent of this challenge, we review the global status and accessibility of ongoing scientific bottom trawl surveys. In total, we gathered metadata for 283,925 samples from 95 surveys conducted regularly from 2001 to 2019. We identified that 59% of the metadata collected are not publicly available, highlighting that the availability of data is the most important challenge to assess species redistributions under global climate change. Given that the primary purpose of surveys is to provide independent data to inform stock assessment of commercially important populations, we further highlight that single surveys do not cover the full range of the main commercial demersal fish species. An average of 18 surveys is needed to cover at least 50% of species ranges, demonstrating the importance of combining multiple surveys to evaluate species range shifts. We assess the potential for combining surveys to track transboundary species redistributions and show that differences in sampling schemes and inconsistency in sampling can be overcome with spatio-temporal modeling to follow species density redistributions. In light of our global assessment, we establish a framework for improving the management and conservation of transboundary and migrating marine demersal species. We provide directions to improve data availability and encourage countries to share survey data, to assess species vulnerabilities, and to support management adaptation in a time of climate-driven ocean changes.

Fish communities diverge in species but converge in traits over three decades of warming.

Describing the spatial and temporal dynamics of communities is essential for understanding the impacts of global environmental change on biodiversity and ecosystem functioning. Trait-based approaches can provide better insight than species-based (i.e. taxonomic) approaches into community assembly and ecosystem functioning, but comparing species and trait dynamics may reveal important patterns for understanding community responses to environmental change. Here, we used a 33-year database of fish monitoring to compare the spatio-temporal dynamics of taxonomic and trait structure in North Sea fish communities. We found that the majority of variation in both taxonomic and trait structure was explained by a pronounced spatial gradient, with distinct communities in the southern and northern North Sea related to depth, sea surface temperature, salinity and bed shear stress. Both taxonomic and trait structure changed significantly over time; however taxonomically, communities in the south and north diverged towards different species, becoming more dissimilar over time, yet they converged towards the same traits regardless of species differences. In particular, communities shifted towards smaller, faster growing species with higher thermal preferences and pelagic water column position. Although taxonomic structure changed over time, its spatial distribution remained relatively stable, whereas in trait structure, the southern zone of the North Sea shifted northward and expanded, leading to homogenization. Our findings suggest that global environmental change, notably climate warming, will lead to convergence towards traits more adapted for novel environments regardless of species composition.

Trait structure and redundancy determine sensitivity to disturbance in marine fish communities.

Trait diversity is believed to influence ecosystem dynamics through links between organismal traits and ecosystem processes. Theory predicts that key traits and high trait redundancy-large species richness and abundance supporting the same traits-can buffer communities against environmental disturbances. While experiments and data from simple ecological systems lend support, large-scale evidence from diverse, natural systems under major disturbance is lacking. Here, using long-term data from both temperate (English Channel) and tropical (Seychelles Islands) fishes, we show that sensitivity to disturbance depends on communities' initial trait structure and initial trait redundancy. In both ecosystems, we found that increasing dominance by climatically vulnerable traits (e.g., small, fast-growing pelagics/corallivores) rendered fish communities more sensitive to environmental change, while communities with higher trait redundancy were more resistant. To our knowledge, this is the first study demonstrating the influence of trait structure and redundancy on community sensitivity over large temporal and spatial scales in natural systems. Our results exemplify a consistent link between biological structure and community sensitivity that may be transferable across ecosystems and taxa and could help anticipate future disturbance impacts on biodiversity and ecosystem functioning.

Functional reorganization of marine fish nurseries under climate warming.

While climate change is rapidly impacting marine species and ecosystems worldwide, the effects of climate warming on coastal fish nurseries have received little attention despite nurseries' fundamental roles in recruitment and population replenishment. Here, we used a 26-year time series (1987-2012) of fish monitoring in the Bay of Somme, a nursery in the Eastern English Channel (EEC), to examine the impacts of environmental and human drivers on the spatial and temporal dynamics of fish functional structure during a warming phase of the Atlantic Multidecadal Oscillation (AMO). We found that the nursery was initially dominated by fishes with r-selected life-history traits such as low trophic level, low age and size at maturity, and small offspring, which are highly sensitive to warming. The AMO, likely superimposed on climate change, induced rapid warming in the late 1990s (over 1°C from 1998 to 2003), leading to functional reorganization of fish communities, with a roughly 80% decline in overall fish abundance and increased dominance by K-selected fishes. Additionally, historical overfishing likely rendered the bay more vulnerable to climatic changes due to increased dominance by fishing-tolerant, yet climatically sensitive species. The drop in fish abundance not only altered fish functional structure within the Bay of Somme, but the EEC was likely impacted, as the EEC has been unable to recover from a regime shift in the late 1990s potentially, in part, due to failed replenishment from the bay. Given the collapse of r-selected fishes, we discuss how the combination of climate cycles and global warming could threaten marine fish nurseries worldwide, as nurseries are often dominated by r-selected species.

A Climate-Driven Functional Inversion of Connected Marine Ecosystems.

Sustainably managing natural resources under climate change requires understanding how species distribution shifts can impact ecosystem structure and functioning. While numerous studies have documented changes in species' distributions and abundances in response to warming [1, 2], the consequences for the functional structure of ecosystems (i.e., composition of species' functional traits) have received less attention. Here, using thirty years of fish monitoring, we show that two connected North Atlantic ecosystems (E. English Channel and S. North Sea) underwent a rapid shift in functional structure triggered by a climate oscillation to a prevailing warm-phase in the late-1990s. Using time-lag-based causality analyses, we found that rapid warming drove pelagic fishes with r-selected life history traits (e.g., low age and size at maturity, small offspring, low trophic level) to shift abruptly northward from one ecosystem to the other, causing an inversion in functional structure between the two connected ecosystems. While we observed only a one-year time-lag between the climate oscillation and the functional shift, indicating rapid responses to a changing environment, historical overfishing likely rendered these ecosystems susceptible to climatic stress [3], and declining fishing in the North Sea may have exacerbated the shift. This shift likely had major consequences for ecosystem functioning due to potential changes in biomass turnover, nutrient cycling, and benthic-pelagic coupling [4-6]. Under ongoing warming, climate oscillations and extreme warming events may increase in frequency and severity [7, 8], which could trigger functional shifts with profound consequences for ecosystem functioning and services.

Regime Shift in an Exploited Fish Community Related to Natural Climate Oscillations.

Identifying the various drivers of marine ecosystem regime shifts and disentangling their respective influence are critical tasks for understanding biodiversity dynamics and properly managing exploited living resources such as marine fish communities. Unfortunately, the mechanisms and forcing factors underlying regime shifts in marine fish communities are still largely unknown although climate forcing and anthropogenic pressures such as fishing have been suggested as key determinants. Based on a 24-year-long time-series of scientific surveys monitoring 55 fish and cephalopods species, we report here a rapid and persistent structural change in the exploited fish community of the eastern English Channel from strong to moderate dominance of small-bodied forage fish species with low temperature preferendum that occurred in the mid-1990s. This shift was related to a concomitant warming of the North Atlantic Ocean as attested by a switch of the Atlantic Multidecadal Oscillation from a cold to a warm phase. Interestingly, observed changes in the fish community structure were opposite to those classically induced by exploitation as larger fish species of higher trophic level increased in abundance. Despite not playing a direct role in the regime shift, fishing still appeared as a forcing factor affecting community structure. Moreover, although related to climate, the regime shift may have been facilitated by strong historic exploitation that certainly primed the system by favoring the large dominance of small-bodied fish species that are particularly sensitive to climatic variations. These results emphasize that particular attention should be paid to multidecadal natural climate variability and its interactions with both fishing and climate warming when aiming at sustainable exploitation and ecosystem conservation.