Scientific impact in a changing world.

Measuring scientific success has traditionally involved numbers and statistics. However, due to an increasingly uncertain world, more than ever we need to measure the effect that science has on real-world scenarios. We asked researchers to share their points of view on what scientific impact means to them and how impact matters beyond the numbers.

Half a century of global decline in oceanic sharks and rays.

Overfishing is the primary cause of marine defaunation, yet declines in and increasing extinction risks of individual species are difficult to measure, particularly for the largest predators found in the high seas1-3. Here we calculate two well-established indicators to track progress towards Aichi Biodiversity Targets and Sustainable Development Goals4,5: the Living Planet Index (a measure of changes in abundance aggregated from 57 abundance time-series datasets for 18 oceanic shark and ray species) and the Red List Index (a measure of change in extinction risk calculated for all 31 oceanic species of sharks and rays). We find that, since 1970, the global abundance of oceanic sharks and rays has declined by 71% owing to an 18-fold increase in relative fishing pressure. This depletion has increased the global extinction risk to the point at which three-quarters of the species comprising this functionally important assemblage are threatened with extinction. Strict prohibitions and precautionary science-based catch limits are urgently needed to avert population collapse6,7, avoid the disruption of ecological functions and promote species recovery8,9.

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.

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.

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.

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.

Maternal Investment, Ecological Lifestyle, and Brain Evolution in Sharks and Rays.

Across vertebrates increased maternal investment (via increased pre- and postnatal provisioning) is associated with larger relative brain size, yet it remains unclear how brain organization is shaped by life history and ecology. Here, we tested whether maternal investment and ecological lifestyle are related to variation in brain size and organization across 100 chondrichthyans. We hypothesized that brain size and organization would vary with the level of maternal investment and habitat depth and complexity. We found that chondrichthyan brain organization varies along four main axes according to (1) absolute brain size, (2) relative diencephalon and mesencephalon size, (3) relative telencephalon and medulla size, and (4) relative cerebellum size. Increased maternal investment is associated with larger relative brain size, while ecological lifestyle is informative for variation between relative telencephalon and medulla size and relative cerebellum size after accounting for the independent effects of reproductive mode. Deepwater chondrichthyans generally provide low levels of yolk-only (lecithotrophic) maternal investment and have relatively small brains, predominantly composed of medulla (a major portion of the hindbrain), whereas matrotrophic chondrichthyans-which provide maternal provisioning beyond the initial yolk sac-found in coastal, reef, or shallow oceanic habitats have relatively large brains, predominantly composed of telencephalon (a major portion of the forebrain). We have demonstrated, for the first time, that both ecological lifestyle and maternal investment are independently associated with brain organization in a lineage with diverse life-history strategies and reproductive modes.

Black-swan events in animal populations.

Black swans are improbable events that nonetheless occur-often with profound consequences. Such events drive important transitions in social systems (e.g., banking collapses) and physical systems (e.g., earthquakes), and yet it remains unclear the extent to which ecological population numbers buffer or suffer from such extremes. Here, we estimate the prevalence and direction of black-swan events (heavy-tailed process noise) in 609 animal populations after accounting for population dynamics (productivity, density dependence, and typical stochasticity). We find strong evidence for black-swan events in [Formula: see text]4% of populations. These events occur most frequently for birds (7%), mammals (5%), and insects (3%) and are not explained by any life-history covariates but tend to be driven by external perturbations such as climate, severe winters, predators, parasites, or the combined effect of multiple factors. Black-swan events manifest primarily as population die-offs and crashes (86%) rather than unexpected increases, and ignoring heavy-tailed process noise leads to an underestimate in the magnitude of population crashes. We suggest modelers consider heavy-tailed, downward-skewed probability distributions, such as the skewed Student [Formula: see text] used here, when making forecasts of population abundance. Our results demonstrate the importance of both modeling heavy-tailed downward events in populations, and developing conservation strategies that are robust to ecological surprises.

Life-history, exploitation and extinction risk of the data-poor Baraka's whipray (Maculabatis ambigua) in small-scale tropical fisheries.

The Baraka's whipray (Maculabatis ambigua) is a major constituent of small-scale fisheries catch in the south-western Indian Ocean. Despite this, little is known of its life-history or exploitation status. We provide the first estimates of crucial life-history parameters and the maximum intrinsic population growth rate rmax , using specimens collected from small-scale fisheries landings in Kenya, Zanzibar and Madagascar (with northern Madagascar representing a range extension for this species). We assess the relative risk of overexploitation by combining rmax with estimates of total Z, fishing F, and natural M mortality, and an estimate of the exploitation ratio E. The data indicate that Baraka's whipray is a medium-sized, fast-growing, early maturing species, with a relatively long lifespan. This results in a high rmax relative to many other elasmobranchs, which when combined with estimates of F suggests that the species is not at imminent risk of extinction. Yet, estimates of exploitation ratio E indicate likely overfishing for the species, with full recruitment to the fishery being post-maturation and exploitation occurring across a broad range of age and size classes. Thus, Baraka's whipray is unlikely to be biologically sustainable in the face of current fisheries pressures. This paper makes an important contribution to filling the gap in available data and is a step towards developing evidence-based fisheries management for this species. Further, it demonstrates a simple and widely applicable framework for assessment of data-poor elasmobranch exploitation status and extinction risk.

Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation.

Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.

The paradox of inverted biomass pyramids in kelp forest fish communities.

Theory predicts that bottom-heavy biomass pyramids or 'stacks' should predominate in real-world communities if trophic-level increases with body size (mean predator-to-prey mass ratio (PPMR) more than 1). However, recent research suggests that inverted biomass pyramids (IBPs) characterize relatively pristine reef fish communities. Here, we estimated the slope of a kelp forest fish community biomass spectrum from underwater visual surveys. The observed biomass spectrum slope is strongly positive, reflecting an IBP. This is incongruous with theory because this steep positive slope would only be expected if trophic position decreased with increasing body size (consumer-to-resource mass ratio, less than 1). We then used δ(15)N signatures of fish muscle tissue to quantify the relationship between trophic position and body size and instead detected strong evidence for the opposite, with PPMR ≈ 1650 (50% credible interval 280-12 000). The natural history of kelp forest reef fishes suggests that this paradox could arise from energetic subsidies in the form of movement of mobile consumers across habitats, and from seasonally pulsed production inputs at small body sizes. There were four to five times more biomass at large body sizes (1-2 kg) than would be expected in a closed steady-state community providing a measure of the magnitude of subsidies.

Clarifying misconceptions of extinction risk assessment with the IUCN Red List.

The identification of species at risk of extinction is a central goal of conservation. As the use of data compiled for IUCN Red List assessments expands, a number of misconceptions regarding the purpose, application and use of the IUCN Red List categories and criteria have arisen. We outline five such classes of misconception; the most consequential drive proposals for adapted versions of the criteria, rendering assessments among species incomparable. A key challenge for the future will be to recognize the point where understanding has developed so markedly that it is time for the next generation of the Red List criteria. We do not believe we are there yet but, recognizing the need for scrutiny and continued development of Red Listing, conclude by suggesting areas where additional research could be valuable in improving the understanding of extinction risk among species.

Energy and the Scaling of Animal Space Use.

Daily animal movements are usually limited to a discrete home range area that scales allometrically with body size, suggesting that home-range size is shaped by metabolic rates and energy availability across species. However, there is little understanding of the relative importance of the various mechanisms proposed to influence home-range scaling (e.g., differences in realm productivity, thermoregulation, locomotion strategy, dimensionality, trophic guild, and prey size) and whether these extend beyond the commonly studied birds and mammals. We derive new home-range scaling relationships for fishes and reptiles and use a model-selection approach to evaluate the generality of home-range scaling mechanisms across 569 vertebrate species. We find no evidence that home-range allometry varies consistently between aquatic and terrestrial realms or thermoregulation strategies, but we find that locomotion strategy, foraging dimension, trophic guild, and prey size together explain 80% of the variation in home-range size across vertebrates when controlling for phylogeny and tracking method. Within carnivores, smaller relative prey size among gape-limited fishes contributes to shallower scaling relative to other predators. Our study reveals how simple morphological traits and prey-handling ability can profoundly influence individual space use, which underpins broader-scale patterns in the spatial ecology of vertebrates.

Portfolio conservation of metapopulations under climate change.

Climate change is likely to lead to increasing population variability and extinction risk. Theoretically, greater population diversity should buffer against rising climate variability, and this theory is often invoked as a reason for greater conservation. However, this has rarely been quantified. Here we show how a portfolio approach to managing population diversity can inform metapopulation conservation priorities in a changing world. We develop a salmon metapopulation model in which productivity is driven by spatially distributed thermal tolerance and patterns of short- and long-term climate change. We then implement spatial conservation scenarios that control population carrying capacities and evaluate the metapopulation portfolios as a financial manager might: along axes of conservation risk and return. We show that preserving a diversity of thermal tolerances minimizes risk, given environmental stochasticity, and ensures persistence, given long-term environmental change. When the thermal tolerances of populations are unknown, doubling the number of populations conserved may nearly halve expected metapopulation variability. However, this reduction in variability can come at the expense of long-term persistence if climate change increasingly restricts available habitat, forcing ecological managers to balance society's desire for short-term stability and long-term viability. Our findings suggest the importance of conserving the processes that promote thermal-tolerance diversity, such as genetic diversity, habitat heterogeneity, and natural disturbance regimes, and demonstrate that diverse natural portfolios may be critical for metapopulation conservation in the face of increasing climate variability and change.

Linking removal targets to the ecological effects of invaders: a predictive model and field test.

Species invasions have a range of negative effects on recipient ecosystems, and many occur at a scale and magnitude that preclude complete eradication. When complete extirpation is unlikely with available management resources, an effective strategy may be to suppress invasive populations below levels predicted to cause undesirable ecological change. We illustrated this approach by developing and testing targets for the control of invasive Indo-Pacific lionfish (Pterois volitans and P. miles) on Western Atlantic coral reefs. We first developed a size-structured simulation model of predation by lionfish on native fish communities, which we used to predict threshold densities of lionfish beyond which native fish biomass should decline. We then tested our predictions by experimentally manipulating lionfish densities above or below reef-specific thresholds, and monitoring the consequences for native fish populations on 24 Bahamian patch reefs over 18 months. We found that reducing lionfish below predicted threshold densities effectively protected native fish community biomass from predation-induced declines. Reductions in density of 25­92%, depending on the reef, were required to suppress lionfish below levels predicted to overconsume prey. On reefs where lionfish were kept below threshold densities, native prey fish biomass increased by 50­70%. Gains in small (<6 cm) size classes of native fishes translated into lagged increases in larger size classes over time. The biomass of larger individuals (>15 cm total length), including ecologically important grazers and economically important fisheries species, had increased by 10­65% by the end of the experiment. Crucially, similar gains in prey fish biomass were realized on reefs subjected to partial and full removal of lionfish, but partial removals took 30% less time to implement. By contrast, the biomass of small native fishes declined by >50% on all reefs with lionfish densities exceeding reef-specific thresholds. Large inter-reef variation in the biomass of prey fishes at the outset of the study, which influences the threshold density of lionfish, means that we could not identify a single rule of thumb for guiding control efforts. However, our model provides a method for setting reef-specific targets for population control using local monitoring data. Our work is the first to demonstrate that for ongoing invasions, suppressing invaders below densities that cause environmental harm can have a similar effect, in terms of protecting the native ecosystem on a local scale, to achieving complete eradication.

Global population trajectories of tunas and their relatives.

Tunas and their relatives dominate the world's largest ecosystems and sustain some of the most valuable fisheries. The impacts of fishing on these species have been debated intensively over the past decade, giving rise to divergent views on the scale and extent of the impacts of fisheries on pelagic ecosystems. We use all available age-structured stock assessments to evaluate the adult biomass trajectories and exploitation status of 26 populations of tunas and their relatives (17 tunas, 5 mackerels, and 4 Spanish mackerels) from 1954 to 2006. Overall, populations have declined, on average, by 60% over the past half century, but the decline in the total adult biomass is lower (52%), driven by a few abundant populations. The trajectories of individual populations depend on the interaction between life histories, ecology, and fishing pressure. The steepest declines are exhibited by two distinct groups: the largest, longest lived, highest value temperate tunas and the smaller, short-lived mackerels, both with most of their populations being overexploited. The remaining populations, mostly tropical tunas, have been fished down to approximately maximum sustainable yield levels, preventing further expansion of catches in these fisheries. Fishing mortality has increased steadily to the point where around 12.5% of the tunas and their relatives are caught each year globally. Overcapacity of these fisheries is jeopardizing their long-term sustainability. To guarantee higher catches, stabilize profits, and reduce collateral impacts on marine ecosystems requires the rebuilding of overexploited populations and stricter management measures to reduce overcapacity and regulate threatening trade.

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.