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.

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.

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.

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.

A global horizon scan of issues impacting marine and coastal biodiversity conservation.

The biodiversity of marine and coastal habitats is experiencing unprecedented change. While there are well-known drivers of these changes, such as overexploitation, climate change and pollution, there are also relatively unknown emerging issues that are poorly understood or recognized that have potentially positive or negative impacts on marine and coastal ecosystems. In this inaugural Marine and Coastal Horizon Scan, we brought together 30 scientists, policymakers and practitioners with transdisciplinary expertise in marine and coastal systems to identify new issues that are likely to have a significant impact on the functioning and conservation of marine and coastal biodiversity over the next 5-10 years. Based on a modified Delphi voting process, the final 15 issues presented were distilled from a list of 75 submitted by participants at the start of the process. These issues are grouped into three categories: ecosystem impacts, for example the impact of wildfires and the effect of poleward migration on equatorial biodiversity; resource exploitation, including an increase in the trade of fish swim bladders and increased exploitation of marine collagens; and new technologies, such as soft robotics and new biodegradable products. Our early identification of these issues and their potential impacts on marine and coastal biodiversity will support scientists, conservationists, resource managers and policymakers to address the challenges facing marine ecosystems.

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.

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.

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.

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.

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.

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.

The timing and causality of ecological shifts on Caribbean reefs.

Caribbean reefs have experienced unprecedented changes in the past four decades. Of great concern is the perceived widespread shift from coral to macroalgal dominance and the question of whether it represents a new, stable equilibrium for coral-reef communities. The primary causes of the shift-grazing pressure (top-down), nutrient loading (bottom-up) or direct coral mortality (side-in)-still remain somewhat controversial in the coral-reef literature. We have attempted to tease out the relative importance of each of these causes. Four insights emerge from our analysis of an early regional dataset of information on the benthic composition of Caribbean reefs spanning the years 1977-2001. First, although three-quarters of reef sites have experienced coral declines concomitant with macroalgal increases, fewer than 10% of the more than 200 sites studied were dominated by macroalgae in 2001, by even the most conservative definition of dominance. Using relative dominance as the threshold, a total of 49 coral-to-macroalgae shifts were detected. This total represents ~35% of all sites that were dominated by coral at the start of their monitoring periods. Four shifts (8.2%) occurred because of coral loss with no change in macroalgal cover, 15 (30.6%) occurred because of macroalgal gain without coral loss, and 30 (61.2%) occurred owing to concomitant coral decline and macroalgal increase. Second, the timing of shifts at the regional scale is most consistent with the side-in model of reef degradation, which invokes coral mortality as a precursor to macroalgal takeover, because more shifts occurred after regional coral-mortality events than expected by chance. Third, instantaneous observations taken at the start and end of the time-series for individual sites showed these reefs existed along a continuum of coral and macroalgal cover. The continuous, broadly negative relationship between coral and macroalgal cover suggests that in some cases coral-to-macroalgae phase shifts may be reversed by removing sources of perturbation or restoring critical components such as the herbivorous sea urchin Diadema antillarum to the system. The five instances in which macroalgal dominance was reversed corroborate the conclusion that macroalgal dominance is not a stable, alternative community state as has been commonly assumed. Fourth, the fact that the loss in regional coral cover and concomitant changes to the benthic community are related to punctuated, discrete events with known causes (i.e. coral disease and bleaching), lends credence to the hypothesis that coral reefs of the Caribbean have been under assault from climate-change-related maladies since the 1970s.

Response to Comment on "Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning".

Allgeier and Cline suggest that our model overestimates the contributions of cryptobenthic fishes to coral reef functioning. However, their 20-year model ignores the basic biological limits of population growth. If incorporated, cryptobenthic contributions to consumed fish biomass remain high (20 to 70%). Disturbance cycles and uncertainties surrounding the fate of large fishes on decadal scales further demonstrate the important role of cryptobenthic fishes.

From individual movement behaviour to landscape-scale invasion dynamics and management: a case study of lionfish metapopulations.

Modelling the dynamics of small, interconnected populations, or metapopulations, can help pinpoint habitat patches that are critical for population persistence in patchy habitats. For conservation purposes, these patches are typically earmarked for protection, but for invasive species management, these patches could be targeted to hasten the populations' demise. Here, we show how metapopulation modelling, coupled with an understanding of size-dependent dispersal behaviour, can be used to help optimize the distribution of limited resources for culling specific populations of invasive Indo-Pacific lionfish (Pterois volitans) in the western Atlantic. Through simulation using fitted model parameters, we derive three insights that can inform management. First, culling lionfish from target patches reduces the probability of lionfish occupancy at surrounding patches. Second, this effect depends on patch size and connectivity, but is strongest at the local scale and decays with distance. Finally, size-dependent dispersal in lionfish means that size-selective culling can change both a population's size distribution and dispersal potential, with cascading effects on network connectivity, population dynamics and management outcomes. By explicitly considering seascape structure and movement behaviour when allocating effort to the management of invasive species, managers can optimize resource use to improve management outcomes. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning.

How coral reefs survive as oases of life in low-productivity oceans has puzzled scientists for centuries. The answer may lie in internal nutrient cycling and/or input from the pelagic zone. Integrating meta-analysis, field data, and population modeling, we show that the ocean's smallest vertebrates, cryptobenthic reef fishes, promote internal reef fish biomass production through extensive larval supply from the pelagic environment. Specifically, cryptobenthics account for two-thirds of reef fish larvae in the near-reef pelagic zone despite limited adult reproductive outputs. This overwhelming abundance of cryptobenthic larvae fuels reef trophodynamics via rapid growth and extreme mortality, producing almost 60% of consumed reef fish biomass. Although cryptobenthics are often overlooked, their distinctive demographic dynamics may make them a cornerstone of ecosystem functioning on modern coral reefs.

Effects of handling and short-term captivity: a multi-behaviour approach using red sea urchins, Mesocentrotus franciscanus.

Understanding the effects of captivity-induced stress on wild-caught animals after their release back into the wild is critical for the long-term success of relocation and reintroduction programs. To date, most of the research on captivity stress has focused on vertebrates, with far less attention paid to invertebrates. Here, we examine the effect of short-term captivity (i.e., up to four days) on self-righting, aggregation, and predator-escape behaviours in wild-caught red sea urchins, Mesocentrotus franciscanus, after their release back into the wild. Aggregation behaviour, which has been linked to feeding in sea urchins, was not affected by handling or captivity. In contrast, the sea urchins that had been handled and released immediately, as well as those that were handled and held captive, took longer to right themselves and were poorer at fleeing from predators than wild, unhandled sea urchins. These results indicate that handling rather than captivity impaired these behaviours in the short term. The duration of captivity did not influence the sea urchin behaviours examined. Longer-term monitoring is needed to establish what the fitness consequences of these short-term behavioural changes might be. Our study nevertheless highlights the importance of considering a suite of responses when examining the effects of capture and captivity. Our findings, which are based on a locally abundant species, can inform translocation efforts aimed at bolstering populations of ecologically similar but depleted invertebrate species to retain or restore important ecosystem functions.

Shifting headlines? Size trends of newsworthy fishes.

The shifting baseline syndrome describes a gradual lowering of human cognitive baselines, as each generation accepts a lower standard of resource abundance or size as the new norm. There is strong empirical evidence of declining trends of abundance and body sizes of marine fish species reported from docks and markets. We asked whether these widespread trends in shrinking marine fish are detectable in popular English-language media, or whether news writers, like many marine stakeholders, are captive to shifting baselines. We collected 266 English-language news articles, printed between 1869 and 2015, which featured headlines that used a superlative adjective, such as 'giant', 'huge', or 'monster', to describe an individual fish caught. We combined the reported sizes of the captured fish with information on maximum species-specific recorded sizes to reconstruct trends of relative size (reported size divided by maximum size) of newsworthy fishes over time. We found some evidence of a shifting baseline syndrome in news media over the last 140 years: overall, the relative length of the largest fish worthy of a headline has declined over time. This pattern held for charismatic fish species (e.g. basking sharks, whale sharks, giant mantas), which are now reported in the media at smaller relative lengths than they were near the turn of the 20th century, and for the largest species under high risk of extinction. In contrast, there was no similar trend for pelagic gamefish and oceanic sharks, or for species under lower risk of extinction. While landing any individual of the large-bodied 'megafish' may be newsworthy in part because of their large size relative to other fish species, the 'megafish' covered in our dataset were small relative to their own species-on average only 56% of the species-specific maximum length. The continued use in the English-language media of superlatives to describe fish that are now a fraction of the maximum size they could reach, or a fraction of the size they used to be, does reflect a shifting baseline for some species. Given that media outlets are a powerful tool for shaping public perception and awareness of environmental issues, there is a real concern that such stories might be interpreted as meaning that superlatively large fish still abound.

Climate Change, Coral Loss, and the Curious Case of the Parrotfish Paradigm: Why Don't Marine Protected Areas Improve Reef Resilience?

Scientists have advocated for local interventions, such as creating marine protected areas and implementing fishery restrictions, as ways to mitigate local stressors to limit the effects of climate change on reef-building corals. However, in a literature review, we find little empirical support for the notion of managed resilience. We outline some reasons for why marine protected areas and the protection of herbivorous fish (especially parrotfish) have had little effect on coral resilience. One key explanation is that the impacts of local stressors (e.g., pollution and fishing) are often swamped by the much greater effect of ocean warming on corals. Another is the sheer complexity (including numerous context dependencies) of the five cascading links assumed by the managed-resilience hypothesis. If reefs cannot be saved by local actions alone, then it is time to face reef degradation head-on, by directly addressing anthropogenic climate change-the root cause of global coral decline.