Author Correction: Global status and conservation potential of reef sharks.

An Amendment to this paper has been published and can be accessed via a link at the top of the paper.

Global status and conservation potential of reef sharks.

Decades of overexploitation have devastated shark populations, leaving considerable doubt as to their ecological status1,2. Yet much of what is known about sharks has been inferred from catch records in industrial fisheries, whereas far less information is available about sharks that live in coastal habitats3. Here we address this knowledge gap using data from more than 15,000 standardized baited remote underwater video stations that were deployed on 371 reefs in 58 nations to estimate the conservation status of reef sharks globally. Our results reveal the profound impact that fishing has had on reef shark populations: we observed no sharks on almost 20% of the surveyed reefs. Reef sharks were almost completely absent from reefs in several nations, and shark depletion was strongly related to socio-economic conditions such as the size and proximity of the nearest market, poor governance and the density of the human population. However, opportunities for the conservation of reef sharks remain: shark sanctuaries, closed areas, catch limits and an absence of gillnets and longlines were associated with a substantially higher relative abundance of reef sharks. These results reveal several policy pathways for the restoration and management of reef shark populations, from direct top-down management of fishing to indirect improvement of governance conditions. Reef shark populations will only have a high chance of recovery by engaging key socio-economic aspects of tropical fisheries.

A marine protected area network does not confer community structure resilience to a marine heatwave across coastal ecosystems.

Marine protected areas (MPAs) have gained attention as a conservation tool for enhancing ecosystem resilience to climate change. However, empirical evidence explicitly linking MPAs to enhanced ecological resilience is limited and mixed. To better understand whether MPAs can buffer climate impacts, we tested the resistance and recovery of marine communities to the 2014-2016 Northeast Pacific heatwave in the largest scientifically designed MPA network in the world off the coast of California, United States. The network consists of 124 MPAs (48 no-take state marine reserves, and 76 partial-take or special regulation conservation areas) implemented at different times, with full implementation completed in 2012. We compared fish, benthic invertebrate, and macroalgal community structure inside and outside of 13 no-take MPAs across rocky intertidal, kelp forest, shallow reef, and deep reef nearshore habitats in California's Central Coast region from 2007 to 2020. We also explored whether MPA features, including age, size, depth, proportion rock, historic fishing pressure, habitat diversity and richness, connectivity, and fish biomass response ratios (proxy for ecological performance), conferred climate resilience for kelp forest and rocky intertidal habitats spanning 28 MPAs across the full network. Ecological communities dramatically shifted due to the marine heatwave across all four nearshore habitats, and MPAs did not facilitate habitat-wide resistance or recovery. Only in protected rocky intertidal habitats did community structure significantly resist marine heatwave impacts. Community shifts were associated with a pronounced decline in the relative proportion of cold water species and an increase in warm water species. MPA features did not explain resistance or recovery to the marine heatwave. Collectively, our findings suggest that MPAs have limited ability to mitigate the impacts of marine heatwaves on community structure. Given that mechanisms of resilience to climate perturbations are complex, there is a clear need to expand assessments of ecosystem-wide consequences resulting from acute climate-driven perturbations, and the potential role of regulatory protection in mitigating community structure changes.

No-take marine protected areas enhance the benefits of kelp-forest restoration for fish but not fisheries.

Kelp habitat restoration is gaining traction as a management action to support recovery in areas affected by severe disturbances, thereby ensuring the sustainability of ecosystem services. Knowing when and where to restore is a major question. Using a single-species population model, we consider how restoring inside marine protected areas (MPAs) might benefit coastal fish populations and fisheries. We found that MPAs can greatly enhance the population benefits of restoration but at a small cost to fishery yields. Generally, restoring inside MPAs had a better overall gains-loss outcome, especially if the system is under high fishing pressure or severe habitat loss. However, restoring outside became preferable when predatory fish indirectly benefit kelp habitats. In either case, successful restoration actions may be difficult to detect in time-series data due to complex transient dynamics. We provide context for setting management goals and social expectations for the ecosystem service implications of restoration in MPAs.

Recruitment variability and sampling design interact to influence the detectability of protected area effects.

Correctly identifying the effects of a human impact on a system is a persistent challenge in ecology, driven partly by the variable nature of natural systems. This is particularly true in many marine fishery species, which frequently experience large temporal fluctuations in recruitment that produce interannual variations in populations. This variability complicates efforts to maintain stocks at management targets or detect the effects of rebuilding efforts. We address this challenge in the context of no-take marine reserves by exploring how variable larval recruitment could interact with the timing of reserve establishment and choice of sampling design to affect population dynamics and the detectability of reserve effects. To predict population changes in the years following a no-take reserve implementation, we first tested for periodicity in larval recruitment in an important U.S. Pacific coast recreational fishery species (kelp bass, Paralabrax clathratus) and then included that pattern in a population model. We also used this model to determine the detectability of population increases under alternative sampling approaches and minimum age sampled. Kelp bass larval recruitment in the Channel Islands, California, peaked every about six (major) and about two (minor) years. Our model showed that establishing a reserve during a peak or trough enhanced or delayed, respectively, the post-reserve population increases. However, establishing a reserve during a recruitment peak could obscure a failing reserve, that is, a reserve that is unable to secure longer-term metapopulation persistence. Recruitment peaks and troughs also interacted with sampling design to affect the detectability of reserve effects. Designs that compared inside-outside were the most robust to variable recruitment, but failed to capture whether the reserve has improved metapopulation growth. Designs that included a time element (e.g., before-after) are more suited to assessing reserve effectiveness, but were sensitive to recruitment variation and detectability can change year-to-year. Notably, detectability did not always increase monotonically with reserve age; the optimal time for detectability depended on the minimum age of organisms sampled and was greatest when the cohort of a major recruitment peak first appeared in the sampling. We encourage managers to account for variable recruitment when planning monitoring and assessment programs.

Grazer behaviour can regulate large-scale patterning of community states.

Ecosystem patterning can arise from environmental heterogeneity, biological feedbacks that produce multiple persistent ecological states, or their interaction. One source of feedbacks is density-dependent changes in behaviour that regulate species interactions. By fitting state-space models to large-scale (~500 km) surveys on temperate rocky reefs, we find that behavioural feedbacks best explain why kelp and urchin barrens form either reef-wide patches or local mosaics. Best-supported models in California include feedbacks where starvation intensifies grazing across entire reefs create reef-scale, alternatively stable kelp- and urchin-dominated states (32% of reefs). Best-fitting models in New Zealand include the feedback of urchins avoiding dense kelp stands that can increase abrasion and predation risk, which drives a transition from shallower urchin-dominated to deeper kelp-dominated zones, with patchiness at 3-8 m depths with intermediate wave stress. Connecting locally studied processes with region-wide data, we highlight how behaviour can explain community patterning and why some systems exhibit community-wide alternative stable states.

Assessing the population-level conservation effects of marine protected areas.

Marine protected areas (MPAs) cover 3-7% of the world's ocean, and international organizations call for 30% coverage by 2030. Although numerous studies show that MPAs produce conservation benefits inside their borders, many MPAs are also justified on the grounds that they confer conservation benefits to the connected populations that span beyond their borders. A network of MPAs covering roughly 20% of the Channel Islands National Marine Sanctuary was established in 2003, with a goal of providing regional conservation and fishery benefits. We used a spatially explicit bioeconomic simulation model and a Bayesian difference-in-difference regression to examine the conditions under which MPAs can provide population-level conservation benefits inside and outside their borders and to assess evidence of those benefits in the Channel Islands. As of 2017, we estimated that biomass densities of targeted fin-fish had a median value 81% higher (90% credible interval: 23-148) inside the Channel Island MPAs than outside. However, we found no clear effect of these MPAs on mean total biomass densities at the population level: estimated median effect was -7% (90% credible interval: -31 to 23) from 2015 to 2017. Our simulation model showed that effect sizes of MPAs of <30% were likely to be difficult to detect (even when they were present); smaller effect sizes (which are likely to be common) were even harder to detect. Clearly, communicating expectations and uncertainties around MPAs is critical to ensuring that MPAs are effective. We provide a novel assessment of the population-level effects of a large MPA network across many different species of targeted fin-fish, and our results offer guidance for communities charged with monitoring and adapting MPAs.

Las áreas marinas protegidas (AMPs) cubren entre 3-7% de los océanos del planeta y las organizaciones internacionales piden una cobertura del 30% para el 2030. Aunque numerosos estudios muestran que las AMPs producen beneficios de conservación dentro de sus límites, muchas de estas áreas también están justificadas por otorgarles beneficios de conservación a las poblaciones conectadas que abarcan más allá de sus fronteras. Una red de AMPs que cubre aproximadamente el 20% del Santuario Marino Nacional de las Islas del Canal fue establecida en 2003 con el objetivo de proporcionar beneficios para la conservación y las pesquerías regionales. Usamos un modelo de simulación bioeconómica espacialmente explícito y una regresión bayesiana de diferencia-en-diferencia para examinar las condiciones bajo las que las AMPs pueden proporcionar beneficios de conservación a nivel poblacional dentro y fuera de sus límites y para evaluar las evidencias de esos beneficios en las Islas del Canal. Hasta el 2017, estimamos que la densidad de la biomasa de los peces focalizados tuvo un valor medio de 81% (90% intervalo creíble 23-148) dentro de las AMPs de las Islas del Canal que fuera de ellas. Sin embargo, no encontramos un efecto claro de estas AMPs sobre la densidad de biomasa total promedio a nivel poblacional; el efecto medio estimado fue de -7% (90% intervalo creíble -31 - 23) entre 2015 y 2017. Nuestro modelo de simulación mostró que los tamaños del efecto de las AMPs menores al 30% tenían mayor probabilidad de ser difíciles de detectar (incluso cuando estaban presentes); los tamaños de efecto más pequeños (que es probable que sean comunes) fueron incluso más difíciles de detectar. Claramente, es muy importante comunicar las expectativas e incertidumbres en torno a las AMPs para asegurar que éstas sean efectivas. Proporcionamos una evaluación novedosa de los efectos a nivel poblacional de una red extensa de AMPs para muchas especies de peces focalizados y nuestros resultados ofrecen una guía para las comunidades encargadas de monitorear y adaptar las AMPs.

Multiyear social stability and social information use in reef sharks with diel fission-fusion dynamics.

Animals across vertebrate taxa form social communities and often exist as fission-fusion groups. Central place foragers (CPF) may form groups from which they will predictably disperse to forage, either individually or in smaller groups, before returning to fuse with the larger group. However, the function and stability of social associations in predatory fish acting as CPFs is unknown, as individuals do not need to return to a shelter yet show fidelity to core areas. Using dynamic social networks generated from acoustic tracking data, we document spatially structured sociality in CPF grey reef sharks at a Pacific Ocean atoll. We show that sharks form stable social groups over multiyear periods, with some dyadic associations consistent for up to 4 years. Groups primarily formed during the day, increasing in size throughout the morning before sharks dispersed from the reef at night. Our simulations suggest that multiple individuals sharing a central place and using social information while foraging (i.e. local enhancement) will outperform non-CPF social foragers. We show multiyear social stability in sharks and suggest that social foraging with information transfer could provide a generalizable mechanism for the emergence of sociality with group central place foraging.

Geographic variation in responses of kelp forest communities of the California Current to recent climatic changes.

The changing global climate is having profound effects on coastal marine ecosystems around the world. Structure, functioning, and resilience, however, can vary geographically, depending on species composition, local oceanographic forcing, and other pressures from human activities and use. Understanding ecological responses to environmental change and predicting changes in the structure and functioning of whole ecosystems require large-scale, long-term studies, yet most studies trade spatial extent for temporal duration. We address this shortfall by integrating multiple long-term kelp forest monitoring datasets to evaluate biogeographic patterns and rates of change of key functional groups (FG) along the west coast of North America. Analysis of data from 469 sites spanning Alaska, USA, to Baja California, Mexico, and 373 species (assigned to 18 FG) reveals regional variation in responses to both long-term (2006-2016) change and a recent marine heatwave (2014-2016) associated with two atmospheric and oceanographic anomalies, the "Blob" and extreme El Niño Southern Oscillation (ENSO). Canopy-forming kelps appeared most sensitive to warming throughout their range. Other FGs varied in their responses among trophic levels, ecoregions, and in their sensitivity to heatwaves. Changes in community structure were most evident within the southern and northern California ecoregions, while communities in the center of the range were more resilient. We report a poleward shift in abundance of some key FGs. These results reveal major, ongoing region-wide changes in productive coastal marine ecosystems in response to large-scale climate variability, and the potential loss of foundation species. In particular, our results suggest that coastal communities that are dependent on kelp forests will be more impacted in the southern portion of the California Current region, highlighting the urgency of implementing adaptive strategies to sustain livelihoods and ensure food security. The results also highlight the value of multiregional integration and coordination of monitoring programs for improving our understanding of marine ecosystems, with the goal of informing policy and resource management in the future.

Habitat-specific inter and intraspecific behavioral interactions among reef sharks.

Behavioral interactions such as dominance are critical components of animal social lives, competitive abilities, and resulting distribution patterns with coexisting species. Strong interference competition can drive habitat separation, but less is known of the role of interference if agonistic interactions are weak. While most theoretical models assume interference abilities to be constant in an environment, few consider that the extent of interference can vary by habitat and change model predictions. Using baited underwater cameras, we show a consistent dominance status between two sympatric reef sharks at an uninhabited Pacific atoll. Blacktip reef shark (Carcharhinus melanopterus) and gray reef shark (Carcharhinus amblyrhyncos) relative abundance showed an inverse relationship to each other but the strength of this relationship varied by habitat. Reef shark relative abundance declined more rapidly in the presence of heterospecifics on forereef habitats as opposed to backreefs. In all habitats, gray reef sharks were more likely to bite bait cages than blacktips when both species were present, and appeared to be the dominant species. Intraspecific interactions were also apparent, with individual willingness to bite bait decreasing as the number of conspecifics increased. Gray reef sharks may exert differential control over blacktip foraging success in different habitats. Habitat-specific behavioral interactions may partially explain patterns of spatial separation between competing species where interference is weak.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

Marine management affects the invasion success of a non-native species in a temperate reef system in California, USA.

Despite promises that 'healthy' marine systems show increased resilience, the effects of ecosystem management strategies on invasion success in marine systems is still unclear. We show that resistance to the invasive alga, Sargassum horneri, in a temperate reef system occurs through alternate mechanisms in different ecosystem states. In an old marine protected area (MPA), invasion of S. horneri was suppressed, likely due to competitive pressure from native algae, resulting from protection of urchin predators. In a nearby fished urchin barren, invasion of S. horneri was also suppressed, due to herbivory by urchins whose predators are fished. Within newer MPAs with intermediate levels of interacting species, S. horneri was abundant. Here, neither competition from native algae nor herbivory was sufficient to prevent invasion. We confirm that invasion in marine systems is complex and show that multiple mechanisms in single systems must be considered when investigating biotic resistance hypotheses.

Mobile marine predators: an understudied source of nutrients to coral reefs in an unfished atoll.

Animal movements can facilitate important ecological processes, and wide-ranging marine predators, such as sharks, potentially contribute significantly towards nutrient transfer between habitats. We applied network theory to 4 years of acoustic telemetry data for grey reef sharks (Carcharhinus amblyrhynchos) at Palmyra, an unfished atoll, to assess their potential role in nutrient dynamics throughout this remote ecosystem. We evaluated the dynamics of habitat connectivity and used network metrics to quantify shark-mediated nutrient distribution. Predator movements were consistent within year, but differed between years and by sex. Females used higher numbers of routes throughout the system, distributing nutrients over a larger proportion of the atoll. Extrapolations of tagged sharks to the population level suggest that prey consumption and subsequent egestion leads to the heterogeneous deposition of 94.5 kg d-1 of nitrogen around the atoll, with approximately 86% of this probably derived from pelagic resources. These results suggest that sharks may contribute substantially to nutrient transfer from offshore waters to near-shore reefs, subsidies that are important for coral reef health.

Size, growth, and density data for shallow-water sea urchins from Mexico to the Aleutian Islands, Alaska, 1956-2016.

Size, growth, and density have been studied for North American Pacific coast sea urchins Strongylocentrotus purpuratus, S. droebachiensis, S. polyacanthus, Mesocentrotus (Strongylocentrotus) franciscanus, Lytechinus pictus, Centrostephanus coronatus, and Arbacia stellata by various workers at diverse sites and for varying lengths of time from 1956 to present. Numerous peer-reviewed publications have used some of these data but some data have appeared only in graduate theses or the gray literature. There also are data that have never appeared outside original data sheets. Motivation for studies has included fisheries management and environmental monitoring of sewer and power plant outfalls as well as changes associated with disease epidemics. Studies also have focused on kelp restoration, community effects of sea otters, basic sea urchin biology, and monitoring. The data sets presented here are a historical record of size, density, and growth for a common group of marine invertebrates in intertidal and nearshore environments that can be used to test hypotheses concerning future changes associated with fisheries practices, shifts of predator distributions, climate and ecosystem changes, and ocean acidification along the Pacific Coast of North America and islands of the north Pacific. No copyright restrictions apply. Please credit this paper when using the data.

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes.

Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2-3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources.

Exploitation and recovery of a sea urchin predator has implications for the resilience of southern California kelp forests.

Size-structured predator-prey interactions can be altered by the history of exploitation, if that exploitation is itself size-selective. For example, selective harvesting of larger sized predators can release prey populations in cases where only large individuals are capable of consuming a particular prey species. In this study, we examined how the history of exploitation and recovery (inside marine reserves and due to fisheries management) of California sheephead (Semicossyphus pulcher) has affected size-structured interactions with sea urchin prey in southern California. We show that fishing changes size structure by reducing sizes and alters life histories of sheephead, while management measures that lessen or remove fishing impacts (e.g. marine reserves, effort restrictions) reverse these effects and result in increases in density, size and biomass. We show that predation on sea urchins is size-dependent, such that the diet of larger sheephead is composed of more and larger sized urchins than the diet of smaller fish. These results have implications for kelp forest resilience, because urchins can overgraze kelp in the absence of top-down control. From surveys in a network of marine reserves, we report negative relationships between the abundance of sheephead and urchins and the abundance of urchins and fleshy macroalgae (including giant kelp), indicating the potential for cascading indirect positive effects of top predators on the abundance of primary producers. Management measures such as increased minimum size limits and marine reserves may serve to restore historical trophic roles of key predators and thereby enhance the resilience of marine ecosystems.

Dietary niche expansion of a kelp forest predator recovering from intense commercial exploitation.

Marine ecosystems are increasingly at risk from overexploitation and fisheries collapse. As managers implement recovery plans, shifts in species interactions may occur broadly with potential consequences for ecosystem structure and function. In kelp forests off San Nicolas Island, California, USA, we describe striking changes in size structure and life history traits (e.g., size at maturation and sex change) of a heavily fished, ecologically important predator, the California sheephead (Semicossyphus pulcher). These changes occurred in two phases: (1) after intense commercial fishery exploitation in the late 1990s and (2) following recovery in the late 2000s, nearly a decade after management intervention. Using gut contents and stable-isotope values of sheephead and their prey, we found evidence for a dietary niche expansion upon recovery of population size structure to include increased consumption of sea urchins and other mobile invertebrate grazers by larger sized fish. By examining historical diet data and a time series of benthic community composition, we conclude that changes in dietary niche breadth are more likely due to the recovery of size structure from fishing than major shifts in prey availability. Size-dependent predator-prey interactions may have ecosystem consequences and management measures that preserve or restore size structure, and therefore historical trophic roles of key predators, could be vital for maintaining kelp forest ecosystem health.

Marine protected area networks in California, USA.

California responded to concerns about overfishing in the 1990s by implementing a network of marine protected areas (MPAs) through two science-based decision-making processes. The first process focused on the Channel Islands, and the second addressed California's entire coastline, pursuant to the state's Marine Life Protection Act (MLPA). We review the interaction between science and policy in both processes, and lessons learned. For the Channel Islands, scientists controversially recommended setting aside 30-50% of coastline to protect marine ecosystems. For the MLPA, MPAs were intended to be ecologically connected in a network, so design guidelines included minimum size and maximum spacing of MPAs (based roughly on fish movement rates), an approach that also implicitly specified a minimum fraction of the coastline to be protected. As MPA science developed during the California processes, spatial population models were constructed to quantify how MPAs were affected by adult fish movement and larval dispersal, i.e., how population persistence within MPA networks depended on fishing outside the MPAs, and how fishery yields could either increase or decrease with MPA implementation, depending on fishery management. These newer quantitative methods added to, but did not supplant, the initial rule-of-thumb guidelines. In the future, similar spatial population models will allow more comprehensive evaluation of the integrated effects of MPAs and conventional fisheries management. By 2011, California had implemented 132 MPAs covering more than 15% of its coastline, and now stands on the threshold of the most challenging step in this effort: monitoring and adaptive management to ensure ecosystem sustainability.

Does fish larval dispersal differ between high and low latitudes?

Several factors lead to expectations that the scale of larval dispersal and population connectivity of marine animals differs with latitude. We examine this expectation for demersal shorefishes, including relevant mechanisms, assumptions and evidence. We explore latitudinal differences in (i) biological (e.g. species composition, spawning mode, pelagic larval duration, PLD), (ii) physical (e.g. water movement, habitat fragmentation), and (iii) biophysical factors (primarily temperature, which could strongly affect development, swimming ability or feeding). Latitudinal differences exist in taxonomic composition, habitat fragmentation, temperature and larval swimming, and each difference could influence larval dispersal. Nevertheless, clear evidence for latitudinal differences in larval dispersal at the level of broad faunas is lacking. For example, PLD is strongly influenced by taxon, habitat and geographical region, but no independent latitudinal trend is present in published PLD values. Any trends in larval dispersal may be obscured by a lack of appropriate information, or use of 'off the shelf' information that is biased with regard to the species assemblages in areas of concern. Biases may also be introduced from latitudinal differences in taxa or spawning modes as well as limited latitudinal sampling. We suggest research to make progress on the question of latitudinal trends in larval dispersal.