Promoting inclusive metrics of success and impact to dismantle a discriminatory reward system in science.

Success and impact metrics in science are based on a system that perpetuates sexist and racist "rewards" by prioritizing citations and impact factors. These metrics are flawed and biased against already marginalized groups and fail to accurately capture the breadth of individuals' meaningful scientific impacts. We advocate shifting this outdated value system to advance science through principles of justice, equity, diversity, and inclusion. We outline pathways for a paradigm shift in scientific values based on multidimensional mentorship and promoting mentee well-being. These actions will require collective efforts supported by academic leaders and administrators to drive essential systemic change.

Anthropogenic pressures and life history predict trajectories of seagrass meadow extent at a global scale.

Seagrass meadows are threatened by multiple pressures, jeopardizing the many benefits they provide to humanity and biodiversity, including climate regulation and food provision through fisheries production. Conservation of seagrass requires identification of the main pressures contributing to loss and the regions most at risk of ongoing loss. Here, we model trajectories of seagrass change at the global scale and show they are related to multiple anthropogenic pressures but that trajectories vary widely with seagrass life-history strategies. Rapidly declining trajectories of seagrass meadow extent (>25% loss from 2000 to 2010) were most strongly associated with high pressures from destructive demersal fishing and poor water quality. Conversely, seagrass meadow extent was more likely to be increasing when these two pressures were low. Meadows dominated by seagrasses with persistent life-history strategies tended to have slowly changing or stable trajectories, while those with opportunistic species were more variable, with a higher probability of either rapidly declining or rapidly increasing. Global predictions of regions most at risk for decline show high-risk areas in Europe, North America, Japan, and southeast Asia, including places where comprehensive long-term monitoring data are lacking. Our results highlight where seagrass loss may be occurring unnoticed and where urgent conservation interventions are required to reverse loss and sustain their essential services.

Interactive effects of multiple stressors vary with consumer interactions, stressor dynamics and magnitude.

Predicting the impacts of multiple stressors is important for informing ecosystem management but is impeded by a lack of a general framework for predicting whether stressors interact synergistically, additively or antagonistically. Here, we use process-based models to study how interactions generalise across three levels of biological organisation (physiological, population and consumer-resource) for a two-stressor experiment on a seagrass model system. We found that the same underlying processes could result in synergistic, additive or antagonistic interactions, with interaction type depending on initial conditions, experiment duration, stressor dynamics and consumer presence. Our results help explain why meta-analyses of multiple stressor experimental results have struggled to identify predictors of consistently non-additive interactions in the natural environment. Experiments run over extended temporal scales, with treatments across gradients of stressor magnitude, are needed to identify the processes that underpin how stressors interact and provide useful predictions to management.

Long-term declines and recovery of meadow area across the world's seagrass bioregions.

As human impacts increase in coastal regions, there is concern that critical habitats that provide the foundation of entire ecosystems are in decline. Seagrass meadows face growing threats such as poor water quality and coastal development. To determine the status of seagrass meadows over time, we reconstructed time series of meadow area from 175 studies that surveyed 547 sites around the world. We found an overall trajectory of decline in all seven bioregions with a global net loss of 5602 km2 (19.1% of surveyed meadow area) occurring since 1880. Declines have typically been non-linear, with rapid and historical losses observed in several bioregions. The greatest net losses of area occurred in four bioregions (Tropical Atlantic, Temperate North Atlantic East, Temperate Southern Oceans and Tropical Indo-Pacific), with declining trends being the slowest and most consistent in the latter two bioregions. In some bioregions, trends have recently stabilised or reversed. Losses, however, still outweigh gains. Despite consistent global declines, meadows show high variability in trajectories, within and across bioregions, highlighting the importance of local context. Studies identified 12 different drivers of meadow area change, with coastal development and water quality as the most commonly cited. Overall, however, attributions were primarily descriptive and only 10% of studies used inferential attributions. Although ours is the most comprehensive dataset to date, it still represents only one-tenth of known global seagrass extent, with conspicuous historical and geographic biases in sampling. It therefore remains unclear whether the bioregional patterns of change documented here reflect changes in the world's unmonitored seagrass meadows. The variability in seagrass meadow trajectories, and the attribution of change to numerous drivers, suggest we urgently need to improve understanding of the causes of seagrass meadow loss if we are to improve local-scale management.

Functional niches of cleanerfish species are mediated by habitat use, cleaning intensity and client selectivity.

An animal's functional niche is a complex, multidimensional construct, mediated by an individual's morphology, physiology and behaviour. Behavioural aspects of the niche can be difficult to quantify, as their expression is often subtle and tailored to an infinite number of different situations that involve sophisticated mechanisms such as mutualisms, species dominance or fear effects. The extreme diversity of tropical fish assemblages has led to extensive debate over the extent to which species differ in their resource use and functional role. Ectoparasite removal by cleanerfish species is considered a behaviourally complex interspecific interaction in vertebrates, but differences in the services rendered by various species of cleanerfish, and potential consequences for the range of clients (i.e. resources) they attract, have rarely been examined. Here, we quantify differences among three coexisting species of morphologically similar cleaner wrasses (Labroides bicolor, L. dimidiatus and L. pectoralis) in the global centre of marine biodiversity, the Coral Triangle. We found no clear taxonomic partitioning of clients among cleanerfishes. However, the three cleanerfish species exhibited distinct habitat preferences, and differed in their cleaning intensity: L. bicolor serviced the fewest species and clients, while L. pectoralis serviced the most clients and spent the most time cleaning. Accordingly, L. pectoralis showed no preference for clients based on client size or abundance, while both L. bicolor and L. dimidiatus had a higher likelihood of interacting with clients based on their size (larger client species in L. bicolor, smaller client species in L. dimidiatus) and abundance (more abundant client species for both). Our results suggest that the services rendered by the three species of cleanerfishes differ in their spatial availability, quality and selectivity, thus permitting the coexistence of these species despite their ecological similarity. This, in turn, creates a complex seascape of species-specific cleaning services that underpins crucial biotic interactions in the ocean's most diverse ecosystem.

Effects of thermal conditioning on the performance of Pocillopora acuta adult coral colonies and their offspring.

Ocean warming induced by climate change is the greatest threat to the persistence of coral reefs globally. Given the current rate of ocean warming, there may not be sufficient time for natural acclimation or adaptation by corals. This urgency has led to the exploration of active management techniques aimed at enhancing thermal tolerance in corals. Here, we test the capacity for transgenerational acclimation in the reef-building coral Pocillopora acuta as a means of increasing offspring performance in warmer waters. We exposed coral colonies from a reef influenced by intermittent upwelling and constant warm-water effluent from a nuclear power plant to temperatures that matched (26 °C) or exceeded (29.5 °C) season-specific mean temperatures for three reproductive cycles; offspring were allowed to settle and grow at both temperatures. Heated colonies reproduced significantly earlier in the lunar cycle and produced fewer and smaller planulae. Recruitment was lower at the heated recruitment temperature regardless of parent treatment. Recruit survival did not differ based on parent or recruitment temperature. Recruits from heated parents were smaller and had lower maximum quantum yield (Fv/Fm), a measurement of symbiont photochemical performance. We found no direct evidence that thermal conditioning of adult P. acuta corals improves offspring performance in warmer water; however, chronic exposure of parent colonies to warmer temperatures at the source reef site may have limited transgenerational acclimation capacity. The extent to which coral response to this active management approach might vary across species and sites remains unclear and merits further investigation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00338-021-02123-9.

Multiple drivers of contrasting diversity-invasibility relationships at fine spatial grains.

The diversity-invasibility hypothesis and ecological theory predict that high-diversity communities should be less easily invaded than species-poor communities, but empirical evidence does not consistently support this prediction. While fine-scale experiments tend to yield the predicted negative association between diversity and invasibility, broad-scale observational surveys generally report a positive correlation. This conflicting pattern between experiments and observational studies is referred to as the invasion paradox and is thought to arise because different processes control species composition at different spatial scales. Here, we test empirically the extent to which the strength and direction of published diversity-invasibility relationships depend on spatial scale and on the metrics used to measure invasibility. Using a meta-analytic framework, we explicitly separate the two components of spatial scale: grain and extent, by focusing on fine-grain studies that vary in extent. We find evidence of multiple drivers of the paradox. When we consider only fine-grain studies, we still observe conflicting patterns between experiments and observational studies. In contrast, when we examine studies that are conducted at both a fine grain and fine extent, there is broad overlap in effect sizes between experiments and observation, suggesting that comparing studies with similar extents resolves the paradox at local scales. However, we uncover systematic differences in the metrics used to measure invasibility between experiments, which use predominantly invader performance, and observational studies, which use mainly invader richness. When we consider studies with the same metric (i.e., invader performance), the contrasting associations between study types also disappear. It is not possible, at present, to fully disentangle the effect of spatial extent and metric on the paradox because both variables are systematically associated in different directions with study type. There is therefore an urgent need to conduct experiments and observational studies that incorporate the full range of variability in spatial extent and invasibility metric.

Interactions among ecosystem stressors and their importance in conservation.

Interactions between multiple ecosystem stressors are expected to jeopardize biological processes, functions and biodiversity. The scientific community has declared stressor interactions-notably synergies-a key issue for conservation and management. Here, we review ecological literature over the past four decades to evaluate trends in the reporting of ecological interactions (synergies, antagonisms and additive effects) and highlight the implications and importance to conservation. Despite increasing popularity, and ever-finer terminologies, we find that synergies are (still) not the most prevalent type of interaction, and that conservation practitioners need to appreciate and manage for all interaction outcomes, including antagonistic and additive effects. However, it will not be possible to identify the effect of every interaction on every organism's physiology and every ecosystem function because the number of stressors, and their potential interactions, are growing rapidly. Predicting the type of interactions may be possible in the near-future, using meta-analyses, conservation-oriented experiments and adaptive monitoring. Pending a general framework for predicting interactions, conservation management should enact interventions that are robust to uncertainty in interaction type and that continue to bolster biological resilience in a stressful world.

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.

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.

Trait-based diet selection: prey behaviour and morphology predict vulnerability to predation in reef fish communities.

Understanding how predators select their prey can provide important insights into community structure and dynamics. However, the suite of prey species available to a predator is often spatially and temporally variable. As a result, species-specific selectivity data are of limited use for predicting novel predator-prey interactions because they are assemblage specific. We present a method for predicting diet selection that is applicable across prey assemblages, based on identifying general morphological and behavioural traits of prey that confer vulnerability to predation independent of species identity. We apply this trait-based approach to examining prey selection by Indo-Pacific lionfish (Pterois volitans and Pterois miles), invasive predators that prey upon species-rich reef fish communities and are rapidly spreading across the western Atlantic. We first generate hypotheses about morphological and behavioural traits recurring across fish species that could facilitate or deter predation by lionfish. Constructing generalized linear mixed-effects models that account for relatedness among prey taxa, we test whether these traits predict patterns of diet selection by lionfish within two independent data sets collected at different spatial scales: (i) in situ visual observations of prey consumption and availability for individual lionfish and (ii) comparisons of prey abundance in lionfish stomach contents to availability on invaded reefs at large. Both analyses reveal that a number of traits predicted to affect vulnerability to predation, including body size, body shape, position in the water column and aggregation behaviour, are important determinants of diet selection by lionfish. Small, shallow-bodied, solitary fishes found resting on or just above reefs are the most vulnerable. Fishes that exhibit parasite cleaning behaviour experience a significantly lower risk of predation than non-cleaning fishes, and fishes that are nocturnally active are at significantly greater risk. Together, vulnerable traits heighten the risk of predation by a factor of nearly 200. Our study reveals that a trait-based approach yields insights into predator-prey interactions that are robust across prey assemblages. Importantly, in situ observations of selection yield similar results to broadscale comparisons of prey use and availability, which are more typically gathered for predator species. A trait-based approach could therefore be of use across predator species and ecosystems to predict the outcomes of changing predator-prey interactions on community dynamics.

Seventy-one important questions for the conservation of marine biodiversity.

The ocean provides food, economic activity, and cultural value for a large proportion of humanity. Our knowledge of marine ecosystems lags behind that of terrestrial ecosystems, limiting effective protection of marine resources. We describe the outcome of 2 workshops in 2011 and 2012 to establish a list of important questions, which, if answered, would substantially improve our ability to conserve and manage the world's marine resources. Participants included individuals from academia, government, and nongovernment organizations with broad experience across disciplines, marine ecosystems, and countries that vary in levels of development. Contributors from the fields of science, conservation, industry, and government submitted questions to our workshops, which we distilled into a list of priority research questions. Through this process, we identified 71 key questions. We grouped these into 8 subject categories, each pertaining to a broad component of marine conservation: fisheries, climate change, other anthropogenic threats, ecosystems, marine citizenship, policy, societal and cultural considerations, and scientific enterprise. Our questions address many issues that are specific to marine conservation, and will serve as a road map to funders and researchers to develop programs that can greatly benefit marine conservation.

Inadvertent consequences of fishing: the case of the sex-changing shrimp.

The Hokkai shrimp Pandalus latirostris starts life as a male, but eventually turns into a female given the right size and social conditions. The traps used in the fishery targeting this species selectively retain the larger females, leaving a severely male-biased sex ratio in nature and social conditions that bear no resemblance to those that prompted (or prevented) sex change. Photo: Susumu Chiba Chiba, S., Yoshino, K., Kanaiwa, M., Kawajiri, T. & Goshima, S. (2013) Maladaptive sex ratio adjustment by a sex-changing shrimp in selective fishing environments. Journal of Animal Ecology, 82, 631-640. Fishing can have many unintended consequences. In this issue, Chiba et al. (2013) demonstrate that size-selective harvesting of a sex-changing shrimp effectively voids their normally adaptive adjustments to population sex ratio. The shrimp's 'decision' to change sex depends largely on the relative abundance of mature males and females in early summer, before fishing begins. However, fishing traps selectively retain females, leading to heavily male-biased sex ratios at the onset of autumn breeding that are different from the ratios that influenced sex-change decisions. Although this phenomenon is not yet expressed in catch trends, maladaptive sex-change decisions could ultimately affect population productivity and persistence.

Abundance modulates the ecosystem functional contributions of two sympatric Caribbean sea cucumbers.

In highly diverse systems such as coral reefs, many species appear to fulfil similar ecological roles, suggesting that they might be ecologically equivalent. However, even if species provide similar functions, the magnitude of those roles could modulate their impact within ecosystems. Here, we compare the functional contributions of two common, co-occurring Caribbean sea cucumber species, Holothuria mexicana and Actynopyga agassizii, in terms of ammonium provisioning and sediment processing on Bahamian patch reefs. We quantified these functions through empirical measures of ammonium excretion, and in situ observations of sediment processing coupled with fecal pellet collections. On a per-individual level, H. mexicana excreted approximately 23% more ammonium and processed approximately 53% more sediment per hour than A. agassizii. However, when we combined these species-specific functional rates to species abundances to produce reef-wide estimates, we found that A. agassizii contributed more than H. mexicana to sediment processing at 57% of reefs (1.9 times more per unit area across all surveyed reefs), and more to ammonium excretion at 83% of reefs (5.6 times more ammonium per unit area across all surveyed reefs), owing to its higher abundance. We conclude that sea cucumber species can differ in the rates at which they deliver per capita ecosystem functions but their ecological impacts at the population level depend on their abundance at a given location.

Functional responses of male and female European green crabs suggest potential sex-specific impacts of invasion.

Predicting the impacts of predatory invasive species is important for prioritising conservation interventions. Functional response experiments, which examine consumption by predators in relation to prey density, are a useful way to assess the potential strength of novel predator-prey relationships. However, such experiments are often conducted without consideration of sex or only with males to reduce invasion risk. Here, we compared the functional responses of male and female European green crabs (Carcinus maenas), a global invader, feeding on varnish clams (Nuttallia obscurata) to test whether the two sexes have similar potential for impact. We also examined potential correlates of predation behaviour by measuring sex-specific movement and prey choice. Both sexes displayed a Type II hyperbolic functional response, which can destabilise prey populations at low prey densities. However, males and females exhibited some differences in foraging behaviour. Female green crabs had slightly lower attack rates, which were not linked to sex differences in movement, and slightly longer handling times, which were not linked to sex differences in prey choice. These small, non-significant differences nevertheless translated into significantly greater functional response ratios, which are used to predict the ecological impact of invasive species, for males than females. There was no difference in the proportion of clams consumed between males and females with similar crusher claw heights, but females have smaller crusher claws on average, hence they consumed a smaller proportion of clams. Repeated surveys of four populations of European green crabs established in British Columbia, Canada, showed that sex ratio is highly variable. Taken together, these results and population-level modelling suggest that trying to evaluate the potential impact of European green crabs on clam populations by sampling only males could result in overestimation, even in populations that have male-biased sex-ratios. Consumer sex might generally be an important feature to consider when using functional response experiments to forecast the impact of new invasive species, especially those with marked sexual dimorphism that affect foraging.

Baseline dynamics of Symbiodiniaceae genera and photochemical efficiency in corals from reefs with different thermal histories.

Ocean warming and marine heatwaves induced by climate change are impacting coral reefs globally, leading to coral bleaching and mortality. Yet, coral resistance and resilience to warming are not uniform across reef sites and corals can show inter- and intraspecific variability. To understand changes in coral health and to elucidate mechanisms of coral thermal tolerance, baseline data on the dynamics of coral holobiont performance under non-stressed conditions are needed. We monitored the seasonal dynamics of algal symbionts (family Symbiodiniaceae) hosted by corals from a chronically warmed and thermally variable reef compared to a thermally stable reef in southern Taiwan over 15 months. We assessed the genera and photochemical efficiency of Symbiodiniaceae in three coral species: Acropora nana, Pocillopora acuta, and Porites lutea. Both Durusdinium and Cladocopium were present in all coral species at both reef sites across all seasons, but general trends in their detection (based on qPCR cycle) varied between sites and among species. Photochemical efficiency (i.e., maximum quantum yield; Fv/Fm) was relatively similar between reef sites but differed consistently among species; no clear evidence of seasonal trends in Fv/Fm was found. Quantifying natural Symbiodiniaceae dynamics can help facilitate a more comprehensive interpretation of thermal tolerance response as well as plasticity potential of the coral holobiont.

A global biological conservation horizon scan of issues for 2023.

We present the results of our 14th horizon scan of issues we expect to influence biological conservation in the future. From an initial set of 102 topics, our global panel of 30 scientists and practitioners identified 15 issues we consider most urgent for societies worldwide to address. Issues are novel within biological conservation or represent a substantial positive or negative step change at global or regional scales. Issues such as submerged artificial light fisheries and accelerating upper ocean currents could have profound negative impacts on marine or coastal ecosystems. We also identified potentially positive technological advances, including energy production and storage, improved fertilisation methods, and expansion of biodegradable materials. If effectively managed, these technologies could realise future benefits for biological diversity.

Evaluating life-history strategies of reef corals from species traits.

Classifying the biological traits of organisms can test conceptual frameworks of life-history strategies and allow for predictions of how different species may respond to environmental disturbances. We apply a trait-based classification approach to a complex and threatened group of species, scleractinian corals. Using hierarchical clustering and random forests analyses, we identify up to four life-history strategies that appear globally consistent across 143 species of reef corals: competitive, weedy, stress-tolerant and generalist taxa, which are primarily separated by colony morphology, growth rate and reproductive mode. Documented shifts towards stress-tolerant, generalist and weedy species in coral reef communities are consistent with the expected responses of these life-history strategies. Our quantitative trait-based approach to classifying life-history strategies is objective, applicable to any taxa and a powerful tool that can be used to evaluate theories of community ecology and predict the impact of environmental and anthropogenic stressors on species assemblages.

Effects of sediment on spore performance as a potential constraint on kelp distribution.

Kelp habitats contribute to marine productivity and diversity, making understanding the constraints on their distribution important. In the Gulf of St. Lawrence, Alaria esculenta occupies a subset of Saccharina latissima's range. Since tolerance to sedimentation by early life stages was suggested to cause this contrasting distribution, we tested the influence of sediment levels on spore attachment and development. For both species, the proportion of attached spores that developed decreased with increasing sediment. However, spore attachment and gametophyte density increased with sediment concentration but only for Saccharina. At the maximum sediment level examined, spore attachment and gametophyte densities of the two species were similar, contrary to the idea that sediment effects on early life stages explain differences in adult distribution. Further investigation, particularly with higher sediment loads, is required to confirm this conclusion. As turbidity is increasing globally, understanding the mechanisms underpinning changes in seaweed distribution will facilitate appropriate local-scale management.