Maternal investment evolves with larger body size and higher diversification rate in sharks and rays.

Across vertebrates, live bearing evolved at least 150 times from ancestral egg laying into diverse forms and degrees of prepartum maternal investment.1,2 A key question is how reproductive diversity arose and whether reproductive diversification underlies species diversification.3,4,5,6,7,8,9,10,11 To test this, we evaluate the most basal jawed vertebrates: the sharks, rays, and chimaeras, which have one of the greatest ranges of reproductive and ecological diversity among vertebrates.2,12 We reconstruct the sequence of reproductive mode evolution across a phylogeny of 610 chondrichthyans.13 We reveal egg laying as ancestral, with live bearing evolving at least seven times. Matrotrophy evolved at least 15 times, with evidence of one reversal. In sharks, transitions to live bearing and matrotrophy are more prevalent in larger-bodied tropical species. Further, the evolution of live bearing is associated with a near doubling of the diversification rate, but there is only a small increase associated with the appearance of matrotrophy. Although pre-copulatory sexual selection is associated with increased rates of speciation in teleosts,3 sexual size dimorphism in chondrichthyans does not appear to be related to sexual selection,14,15 and instead we find increased rates of speciation associated with the colonization of novel habitats. This highlights a potential key difference between chondrichthyans and other fishes, specifically a slower rate of evolution of reproductive isolation following speciation, suggesting different rate-limiting mechanisms for diversification between these clades.16 The chondrichthyan diversification and radiation, particularly throughout shallow tropical shelf seas and oceanic pelagic habitats, appear to be associated with the evolution of live bearing and proliferation of a wide range of maternal investment in developing offspring.

Fishing for oil and meat drives irreversible defaunation of deepwater sharks and rays.

The deep ocean is the last natural biodiversity refuge from the reach of human activities. Deepwater sharks and rays are among the most sensitive marine vertebrates to overexploitation. One-third of threatened deepwater sharks are targeted, and half the species targeted for the international liver-oil trade are threatened with extinction. Steep population declines cannot be easily reversed owing to long generation lengths, low recovery potentials, and the near absence of management. Depth and spatial limits to fishing activity could improve conservation when implemented alongside catch regulations, bycatch mitigation, and international trade regulation. Deepwater sharks and rays require immediate trade and fishing regulations to prevent irreversible defaunation and promote recovery of this threatened megafauna group.

Size-dependence of food intake and mortality interact with temperature and seasonality to drive diversity in fish life histories.

Understanding how growth and reproduction will adapt to changing environmental conditions is a fundamental question in evolutionary ecology, but predicting the responses of specific taxa is challenging. Analyses of the physiological effects of climate change upon life history evolution rarely consider alternative hypothesized mechanisms, such as size-dependent foraging and the risk of predation, simultaneously shaping optimal growth patterns. To test for interactions between these mechanisms, we embedded a state-dependent energetic model in an ecosystem size-spectrum to ask whether prey availability (foraging) and risk of predation experienced by individual fish can explain observed diversity in life histories of fishes. We found that asymptotic growth emerged from size-based foraging and reproductive and mortality patterns in the context of ecosystem food web interactions. While more productive ecosystems led to larger body sizes, the effects of temperature on metabolic costs had only small effects on size. To validate our model, we ran it for abiotic scenarios corresponding to the ecological lifestyles of three tuna species, considering environments that included seasonal variation in temperature. We successfully predicted realistic patterns of growth, reproduction, and mortality of all three tuna species. We found that individuals grew larger when environmental conditions varied seasonally, and spawning was restricted to part of the year (corresponding to their migration from temperate to tropical waters). Growing larger was advantageous because foraging and spawning opportunities were seasonally constrained. This mechanism could explain the evolution of gigantism in temperate tunas. Our approach addresses variation in food availability and individual risk as well as metabolic processes and offers a promising approach to understand fish life-history responses to changing ocean conditions.

A multi-taxon analysis of European Red Lists reveals major threats to biodiversity.

Biodiversity loss is a major global challenge and minimizing extinction rates is the goal of several multilateral environmental agreements. Policy decisions require comprehensive, spatially explicit information on species' distributions and threats. We present an analysis of the conservation status of 14,669 European terrestrial, freshwater and marine species (ca. 10% of the continental fauna and flora), including all vertebrates and selected groups of invertebrates and plants. Our results reveal that 19% of European species are threatened with extinction, with higher extinction risks for plants (27%) and invertebrates (24%) compared to vertebrates (18%). These numbers exceed recent IPBES (Intergovernmental Platform on Biodiversity and Ecosystem Services) assumptions of extinction risk. Changes in agricultural practices and associated habitat loss, overharvesting, pollution and development are major threats to biodiversity. Maintaining and restoring sustainable land and water use practices is crucial to minimize future biodiversity declines.

Tail shape and the swimming speed of sharks.

Trait-based ecology is a rapidly growing approach for developing insights and predictions for data-poor species. Caudal tail fin shape has the potential to reveal much about the energetics, activity and ecology of fishes and can be rapidly measured from field guides, which is particularly helpful for data-sparse species. One outstanding question is whether swimming speed in sharks is related to two morphological traits: caudal fin aspect ratio (CFAR, height2/tail area) and caudal lobe asymmetry ratio (CLAR). We derived both metrics from the species drawings in Sharks of the world (Ebert et al. 2013 Sharks of the world: a fully illustrated guide) and related fin shape to two published datasets of (1) instantaneous swimming speeds (Jacoby et al. 2015 Biol. Lett. 11, 20150781 (doi:10.1098/rsbl.2015.0781)) and (2) cruising speeds (Harding et al. 2021 Funct. Ecol. 35, 1951-1959 (doi:10.1111/1365-2435.13869)) for 28 total unique shark species. Both estimates of swimming speed were positively related to CFAR (and weakly negatively to CLAR). Hence, shark species with larger CFAR and more symmetric tails (low CLAR) tended to be faster-moving and have higher average speeds. This relationship demonstrates the opportunity to use tail shape as an easily measured trait to index shark swimming speed to broader trait-based analyses of ecological function and extinction risk.

The allometric scaling of oxygen supply and demand in the California horn shark, Heterodontus francisci.

The gill surface area of aquatic ectotherms is thought to be closely linked to the ontogenetic scaling of metabolic rate, a relationship that is often used to explain and predict ecological patterns across species. However, there are surprisingly few within-species tests of whether metabolic rate and gill area scale similarly. We examined the relationship between oxygen supply (gill area) and demand (metabolic rate) by making paired estimates of gill area with resting and maximum metabolic rates across ontogeny in the relatively inactive California horn shark, Heterodontus francisci. We found that the allometric slope of resting metabolic rate was 0.966±0.058 (±95% CI), whereas that of maximum metabolic rate was somewhat steeper (1.073±0.040). We also discovered that the scaling of gill area shifted with ontogeny: the allometric slope of gill area was shallower in individuals <0.203 kg in body mass (0.564±0.261), but increased to 1.012±0.113 later in life. This appears to reflect changes in demand for gill-oxygen uptake during egg case development and immediately post hatch, whereas for most of ontogeny, gill area scales in between that of resting and maximum metabolic rate. These relationships differ from predictions of the gill oxygen limitation theory, which argues that the allometric scaling of gill area constrains metabolic processes. Thus, for the California horn shark, metabolic rate does not appear limited by theoretical surface-area-to-volume ratio constraints of gill area. These results highlight the importance of data from paired and size-matched individuals when comparing physiological scaling relationships.

Half a century of rising extinction risk of coral reef sharks and rays.

Sharks and rays are key functional components of coral reef ecosystems, yet many populations of a few species exhibit signs of depletion and local extinctions. The question is whether these declines forewarn of a global extinction crisis. We use IUCN Red List to quantify the status, trajectory, and threats to all coral reef sharks and rays worldwide. Here, we show that nearly two-thirds (59%) of the 134 coral-reef associated shark and ray species are threatened with extinction. Alongside marine mammals, sharks and rays are among the most threatened groups found on coral reefs. Overfishing is the main cause of elevated extinction risk, compounded by climate change and habitat degradation. Risk is greatest for species that are larger-bodied (less resilient and higher trophic level), widely distributed across several national jurisdictions (subject to a patchwork of management), and in nations with greater fishing pressure and weaker governance. Population declines have occurred over more than half a century, with greatest declines prior to 2005. Immediate action through local protections, combined with broad-scale fisheries management and Marine Protected Areas, is required to avoid extinctions and the loss of critical ecosystem function condemning reefs to a loss of shark and ray biodiversity and ecosystem services, limiting livelihoods and food security.

Conservation successes and challenges for wide-ranging sharks and rays.

Overfishing is the most significant threat facing sharks and rays. Given the growth in consumption of seafood, combined with the compounding effects of habitat loss, climate change, and pollution, there is a need to identify recovery paths, particularly in poorly managed and poorly monitored fisheries. Here, we document conservation through fisheries management success for 11 coastal sharks in US waters by comparing population trends through a Bayesian state-space model before and after the implementation of the 1993 Fisheries Management Plan for Sharks. We took advantage of the spatial and temporal gradients in fishing exposure and fisheries management in the Western Atlantic to analyze the effect on the Red List status of all 26 wide-ranging coastal sharks and rays. We show that extinction risk was greater where fishing pressure was higher, but this was offset by the strength of management engagement (indicated by strength of National and Regional Plan of Action for sharks and rays). The regional Red List Index (which tracks changes in extinction risk through time) declined in all regions until the 1980s but then improved in the North and Central Atlantic such that the average extinction risk is currently half that in the Southwest. Many sharks and rays are wide ranging, and successful fisheries management in one country can be undone by poorly regulated or unregulated fishing elsewhere. Our study underscores that well-enforced, science-based management of carefully monitored fisheries can achieve conservation success, even for slow-growing species.

Seventy years of tunas, billfishes, and sharks as sentinels of global ocean health.

Fishing activity is closely monitored to an increasing degree, but its effects on biodiversity have not received such attention. Using iconic and well-studied fish species such as tunas, billfishes, and sharks, we calculate a continuous Red List Index of yearly changes in extinction risk over 70 years to track progress toward global sustainability and biodiversity targets. We show that this well-established biodiversity indicator is highly sensitive and responsive to fishing mortality. After ~58 years of increasing risk of extinction, effective fisheries management has shifted the biodiversity loss curve for tunas and billfishes, whereas the curve continues to worsen for sharks, which are highly undermanaged. While populations of highly valuable commercial species are being rebuilt, the next management challenge is to halt and reverse the harm afflicted by these same fisheries to broad oceanic biodiversity.

Body mass, temperature, and depth shape the maximum intrinsic rate of population increase in sharks and rays.

An important challenge in ecology is to understand variation in species' maximum intrinsic rate of population increase, r max , not least because r max underpins our understanding of the limits of fishing, recovery potential, and ultimately extinction risk. Across many vertebrate species, terrestrial and aquatic, body mass and environmental temperature are important correlates of r max . In sharks and rays, specifically, r max is known to be lower in larger species, but also in deep sea ones. We use an information-theoretic approach that accounts for phylogenetic relatedness to evaluate the relative importance of body mass, temperature, and depth on r max . We show that both temperature and depth have separate effects on shark and ray r max estimates, such that species living in deeper waters have lower r max . Furthermore, temperature also correlates with changes in the mass scaling coefficient, suggesting that as body size increases, decreases in r max are much steeper for species in warmer waters. These findings suggest that there are (as-yet understood) depth-related processes that limit the maximum rate at which populations can grow in deep-sea sharks and rays. While the deep ocean is associated with colder temperatures, other factors that are independent of temperature, such as food availability and physiological constraints, may influence the low r max observed in deep-sea sharks and rays. Our study lays the foundation for predicting the intrinsic limit of fishing, recovery potential, and extinction risk species based on easily accessible environmental information such as temperature and depth, particularly for data-poor species.

Sharkipedia: a curated open access database of shark and ray life history traits and abundance time-series.

A curated database of shark and ray biological data is increasingly necessary both to support fisheries management and conservation efforts, and to test the generality of hypotheses of vertebrate macroecology and macroevolution. Sharks and rays are one of the most charismatic, evolutionary distinct, and threatened lineages of vertebrates, comprising around 1,250 species. To accelerate shark and ray conservation and science, we developed Sharkipedia as a curated open-source database and research initiative to make all published biological traits and population trends accessible to everyone. Sharkipedia hosts information on 58 life history traits from 274 sources, for 170 species, from 39 families, and 12 orders related to length (n = 9 traits), age (8), growth (12), reproduction (19), demography (5), and allometric relationships (5), as well as 871 population time-series from 202 species. Sharkipedia relies on the backbone taxonomy of the IUCN Red List and the bibliography of Shark-References. Sharkipedia has profound potential to support the rapidly growing data demands of fisheries management, international trade regulation as well as anchoring vertebrate macroecology and macroevolution.

Current and future considerations for shark conservation in the Northeast and Eastern Central Pacific Ocean.

Sharks are iconic and ecologically important predators found in every ocean. Because of their ecological role as predators, some considered apex predators, and concern over the stability of their populations due to direct and indirect overfishing, there has been an increasing amount of work focussed on shark conservation, and other elasmobranchs such as skates and rays, around the world. Here we discuss many aspects of current shark science and conservation and the path to the future of shark conservation in the Northeastern and Eastern Central Pacific. We explore their roles in ecosystems as keystone species; the conservation measures and laws in place at the international, national, regional and local level; the conservation status of sharks and rays in the region, fisheries for sharks in the Northcentral Pacific specifically those that target juveniles and the implications to shark conservation; a conservation success story: the recovery of Great White Sharks in the Northeast Pacific; public perceptions of sharks and the roles zoos and aquariums play in shark conservation; and the path to the future of shark conservation that requires bold partnerships, local stakeholders and innovative measures.

Overfishing drives over one-third of all sharks and rays toward a global extinction crisis.

The scale and drivers of marine biodiversity loss are being revealed by the International Union for Conservation of Nature (IUCN) Red List assessment process. We present the first global reassessment of 1,199 species in Class Chondrichthyes-sharks, rays, and chimeras. The first global assessment (in 2014) concluded that one-quarter (24%) of species were threatened. Now, 391 (32.6%) species are threatened with extinction. When this percentage of threat is applied to Data Deficient species, more than one-third (37.5%) of chondrichthyans are estimated to be threatened, with much of this change resulting from new information. Three species are Critically Endangered (Possibly Extinct), representing possibly the first global marine fish extinctions due to overfishing. Consequently, the chondrichthyan extinction rate is potentially 25 extinctions per million species years, comparable to that of terrestrial vertebrates. Overfishing is the universal threat affecting all 391 threatened species and is the sole threat for 67.3% of species and interacts with three other threats for the remaining third: loss and degradation of habitat (31.2% of threatened species), climate change (10.2%), and pollution (6.9%). Species are disproportionately threatened in tropical and subtropical coastal waters. Science-based limits on fishing, effective marine protected areas, and approaches that reduce or eliminate fishing mortality are urgently needed to minimize mortality of threatened species and ensure sustainable catch and trade of others. Immediate action is essential to prevent further extinctions and protect the potential for food security and ecosystem functions provided by this iconic lineage of predators.

Analytical methods matter too: Establishing a framework for estimating maximum metabolic rate for fishes.

Advances in experimental design and equipment have simplified the collection of maximum metabolic rate (MMR) data for a more diverse array of water-breathing animals. However, little attention has been given to the consequences of analytical choices in the estimation of MMR. Using different analytical methods can reduce the comparability of MMR estimates across species and studies and has consequences for the burgeoning number of macroecological meta-analyses using metabolic rate data. Two key analytical choices that require standardization are the time interval, or regression window width, over which MMR is estimated, and the method used to locate that regression window within the raw oxygen depletion trace. Here, we consider the effect of both choices by estimating MMR for two shark and two salmonid species of different activity levels using multiple regression window widths and three analytical methods: rolling regression, sequential regression, and segmented regression. Shorter regression windows yielded higher metabolic rate estimates, with a risk that the shortest windows (<1-min) reflect more system noise than MMR signal. Rolling regression was the best candidate model and produced the highest MMR estimates. Sequential regression models consistently produced lower relative estimates than rolling regression models, while the segmented regression model was unable to produce consistent MMR estimates across individuals. The time-point of the MMR regression window along the oxygen consumption trace varied considerably across individuals but not across models. We show that choice of analytical method, in addition to more widely understood experimental choices, profoundly affect the resultant estimates of MMR. We recommend that researchers (1) employ a rolling regression model with a reliable regression window tailored to their experimental system and (2) explicitly report their analytical methods, including publishing raw data and code.

The role and value of science in shark conservation advocacy.

Many species of sharks are threatened with extinction, and there has been a longstanding debate in scientific and environmental circles over the most effective and appropriate strategy to conserve and protect them. Should we allow for sustainable fisheries exploitation of species which can withstand fishing pressure, or ban all fisheries for sharks and trade in shark products? In the developing world, exploitation of fisheries resources can be essential to food security and poverty alleviation, and global management efforts are typically focused on sustainably maximizing economic benefits. This approach aligns with traditional fisheries management and the perspectives of most surveyed scientific researchers who study sharks. However, in Europe and North America, sharks are increasingly venerated as wildlife to be preserved irrespective of conservation status, resulting in growing pressure to prohibit exploitation of sharks and trade in shark products. To understand the causes and significance of this divergence in goals, we surveyed 155 shark conservation focused environmental advocates from 78 environmental non-profits, and asked three key questions: (1) where do advocates get scientific information? (2) Does all policy-relevant scientific information reach advocates? and (3) Do advocates work towards the same policy goals identified by scientific researchers? Findings suggest many environmental advocates are aware of key scientific results and use science-based arguments in their advocacy, but a small but vocal subset of advocates report that they never read the scientific literature or speak to scientists. Engagement with science appears to be a key predictor of whether advocates support sustainable management of shark fisheries or bans on shark fishing and trade in shark products. Conservation is a normative discipline, and this analysis more clearly articulates two distinct perspectives in shark conservation. Most advocates support the same evidence-based policies as academic and government scientists, while a smaller percentage are driven more by moral and ethical beliefs and may not find scientific research relevant or persuasive. We also find possible evidence that a small group of non-profits may be misrepresenting the state of the science while claiming to use science-based arguments, a concern that has been raised by surveyed scientists about the environmental community. This analysis suggests possible alternative avenues for engaging diverse stakeholders in productive discussions about shark conservation.

Tracking the rising extinction risk of sharks and rays in the Northeast Atlantic Ocean and Mediterranean Sea.

The loss of biodiversity is increasingly well understood on land, but trajectories of extinction risk remain largely unknown in the ocean. We present regional Red List Indices (RLIs) to track the extinction risk of 119 Northeast Atlantic and 72 Mediterranean shark and ray species primarily threatened by overfishing. We combine two IUCN workshop assessments from 2003/2005 and 2015 with a retrospective backcast assessment for 1980. We incorporate predicted categorisations for Data Deficient species from our previously published research. The percentage of threatened species rose from 1980 to 2015 from 29 to 41% (Northeast Atlantic) and 47 to 65% (Mediterranean Sea). There are as many threatened sharks and rays in Europe as there are threatened birds, but the threat level is nearly six times greater by percentage (41%, n = 56 of 136 vs. 7%, n = 56 of 792). The Northeast Atlantic RLI declined by 8% from 1980 to 2015, while the higher-risk Mediterranean RLI declined by 13%. Larger-bodied, shallow-distributed, slow-growing species and those with range boundaries within the region are more likely to have worsening status in the Northeast Atlantic. Conversely, long-established, severe threat levels obscure any potential relationships between species' traits and the likelihood of worsening IUCN status in the Mediterranean Sea. These regional RLIs provide the first widespread evidence for increasing trends in regional shark and ray extinction risk and underscore that effective fisheries management is necessary to recover the ecosystem function of these predators.

The metabolic pace of life histories across fishes.

All life acquires energy through metabolic processes and that energy is subsequently allocated to life-sustaining functions such as survival, growth and reproduction. Thus, it has long been assumed that metabolic rate is related to the life history of an organism. Indeed, metabolic rate is commonly believed to set the pace of life by determining where an organism is situated along a fast-slow life-history continuum. However, empirical evidence of a direct interspecific relationship between metabolic rate and life histories is lacking, especially for ectothermic organisms. Here, we ask whether three life-history traits-maximum body mass, generation length and growth performance-explain variation in resting metabolic rate (RMR) across fishes. We found that growth performance, which accounts for the trade-off between growth rate and maximum body size, explained variation in RMR, yet maximum body mass and generation length did not. Our results suggest that measures of life history that encompass trade-offs between life-history traits, rather than traits in isolation, explain variation in RMR across fishes. Ultimately, understanding the relationship between metabolic rate and life history is crucial to metabolic ecology and has the potential to improve prediction of the ecological risk of data-poor species.

Respiratory capacity is twice as important as temperature in explaining patterns of metabolic rate across the vertebrate tree of life.

Metabolic rate underlies a wide range of phenomena from cellular dynamics to ecosystem structure and function. Models seeking to statistically explain variation in metabolic rate across vertebrates are largely based on body size and temperature. Unexpectedly, these models overlook variation in the size of gills and lungs that acquire the oxygen needed to fuel aerobic processes. Here, we assess the importance of respiratory surface area in explaining patterns of metabolic rate across the vertebrate tree of life using a novel phylogenetic Bayesian multilevel modeling framework coupled with a species-paired dataset of metabolic rate and respiratory surface area. We reveal that respiratory surface area explains twice as much variation in metabolic rate, compared to temperature, across the vertebrate tree of life. Understanding the combination of oxygen acquisition and transport provides opportunity to understand the evolutionary history of metabolic rate and improve models that quantify the impacts of climate change.

Gill surface area provides a clue for the respiratory basis of brain size in the blacktip shark (Carcharhinus limbatus).

Brain size varies dramatically, both within and across species, and this variation is often believed to be the result of trade-offs between the cognitive benefits of having a large brain for a given body size and the energetic cost of sustaining neural tissue. One potential consequence of having a large brain is that organisms must also meet the associated high energetic demands. Thus, a key question is whether metabolic rate correlates with brain size. However, using metabolic rate to measure energetic demand yields a relatively instantaneous and dynamic measure of energy turnover, which is incompatible with the longer evolutionary timescale of changes in brain size within and across species. Morphological traits associated with oxygen consumption, specifically gill surface area, have been shown to be correlates of oxygen demand and energy use, and thus may serve as integrated correlates of these processes, allowing us to assess whether evolutionary changes in brain size correlate with changes in longer-term oxygen demand and energy use. We tested how brain size relates to gill surface area in the blacktip shark Carcharhinus limbatus. First, we examined whether the allometric slope of brain mass (i.e., the rate that brain mass changes with body mass) is lower than the allometric slope of gill surface area across ontogeny. Second, we tested whether gill surface area explains variation in brain mass, after accounting for the effects of body mass on brain mass. We found that brain mass and gill surface area both had positive allometric slopes, with larger individuals having both larger brains and larger gill surface areas compared to smaller individuals. However, the allometric slope of brain mass was lower than the allometric slope of gill surface area, consistent with our prediction that the allometric slope of gill surface area could pose an upper limit to the allometric slope of brain mass. Finally, after accounting for body mass, individuals with larger brains tended to have larger gill surface areas. Together, our results provide clues as to how fishes may evolve and maintain large brains despite their high energetic cost, suggesting that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover, and, in turn, a larger brain for their body mass.