Directed conservation of the world's reef sharks and rays.

Many shark populations are in decline around the world, with severe ecological and economic consequences. Fisheries management and marine protected areas (MPAs) have both been heralded as solutions. However, the effectiveness of MPAs alone is questionable, particularly for globally threatened sharks and rays ('elasmobranchs'), with little known about how fisheries management and MPAs interact to conserve these species. Here we use a dedicated global survey of coral reef elasmobranchs to assess 66 fully protected areas embedded within a range of fisheries management regimes across 36 countries. We show that conservation benefits were primarily for reef-associated sharks, which were twice as abundant in fully protected areas compared with areas open to fishing. Conservation benefits were greatest in large protected areas that incorporate distinct reefs. However, the same benefits were not evident for rays or wide-ranging sharks that are both economically and ecologically important while also threatened with extinction. We show that conservation benefits from fully protected areas are close to doubled when embedded within areas of effective fisheries management, highlighting the importance of a mixed management approach of both effective fisheries management and well-designed fully protected areas to conserve tropical elasmobranch assemblages globally.

Links between the three-dimensional movements of whale sharks (Rhincodon typus) and the bio-physical environment off a coral reef.

BACKGROUND: Measuring coastal-pelagic prey fields at scales relevant to the movements of marine predators is challenging due to the dynamic and ephemeral nature of these environments. Whale sharks (Rhincodon typus) are thought to aggregate in nearshore tropical waters due to seasonally enhanced foraging opportunities. This implies that the three-dimensional movements of these animals may be associated with bio-physical properties that enhance prey availability. To date, few studies have tested this hypothesis. METHODS: Here, we conducted ship-based acoustic surveys, net tows and water column profiling (salinity, temperature, chlorophyll fluorescence) to determine the volumetric density, distribution and community composition of mesozooplankton (predominantly euphausiids and copepods) and oceanographic properties of the water column in the vicinity of whale sharks that were tracked simultaneously using satellite-linked tags at Ningaloo Reef, Western Australia. Generalised linear mixed effect models were used to explore relationships between the 3-dimensional movement behaviours of tracked sharks and surrounding prey fields at a spatial scale of ~ 1 km. RESULTS: We identified prey density as a significant driver of horizontal space use, with sharks occupying areas along the reef edge where densities were highest. These areas were characterised by complex bathymetry such as reef gutters and pinnacles. Temperature and salinity profiles revealed a well-mixed water column above the height of the bathymetry (top 40 m of the water column). Regions of stronger stratification were associated with reef gutters and pinnacles that concentrated prey near the seabed, and entrained productivity at local scales (~ 1 km). We found no quantitative relationship between the depth use of sharks and vertical distributions of horizontally averaged prey density. Whale sharks repeatedly dove to depths where spatially averaged prey concentration was highest but did not extend the time spent at these depth layers. CONCLUSIONS: Our work reveals previously unrecognized complexity in interactions between whale sharks and their zooplankton prey.

A large-scale experiment finds no consistent evidence of change in mortality or commercial productivity in silverlip pearl oysters (Pinctada maxima) exposed to a seismic source survey.

High-intensity, impulsive sounds are used to locate oil and gas reserves during seismic exploration of the seafloor. The impacts of this noise pollution on the health and mortality of marine invertebrates are not well known, including the silverlip pearl oyster (Pinctada maxima), which comprises one of the world's last remaining significant wildstock pearl oyster fisheries, in northwestern Australia. We exposed ≈11,000 P. maxima to a four-day experimental seismic survey, plus one vessel-control day. After exposure, survival rates were monitored throughout a full two-year production cycle, and the number and quality of pearls produced at harvest were assessed. Oysters from two groups, on one sampling day, exhibited reduced survival and pearl productivity compared to controls, but 14 other groups receiving similar or higher exposure levels did not. We therefore found no conclusive evidence of an impact of the seismic source survey on oyster mortality or pearl production.

Widespread diversity deficits of coral reef sharks and rays.

A global survey of coral reefs reveals that overfishing is driving resident shark species toward extinction, causing diversity deficits in reef elasmobranch (shark and ray) assemblages. Our species-level analysis revealed global declines of 60 to 73% for five common resident reef shark species and that individual shark species were not detected at 34 to 47% of surveyed reefs. As reefs become more shark-depleted, rays begin to dominate assemblages. Shark-dominated assemblages persist in wealthy nations with strong governance and in highly protected areas, whereas poverty, weak governance, and a lack of shark management are associated with depauperate assemblages mainly composed of rays. Without action to address these diversity deficits, loss of ecological function and ecosystem services will increasingly affect human communities.

Wearable sensors for monitoring marine environments and their inhabitants.

Human societies depend on marine ecosystems, but their degradation continues. Toward mitigating this decline, new and more effective ways to precisely measure the status and condition of marine environments are needed alongside existing rebuilding strategies. Here, we provide an overview of how sensors and wearable technology developed for humans could be adapted to improve marine monitoring. We describe barriers that have slowed the transition of this technology from land to sea, update on the developments in sensors to advance ocean observation and advocate for more widespread use of wearables on marine organisms in the wild and in aquaculture. We propose that large-scale use of wearables could facilitate the concept of an 'internet of marine life' that might contribute to a more robust and effective observation system for the oceans and commercial aquaculture operations. These observations may aid in rationalizing strategies toward conservation and restoration of marine communities and habitats.

Free-diving sharks.

Hammerhead sharks hold their breath when diving to regulate body temperature.

Scaling of Activity Space in Marine Organisms across Latitudinal Gradients.

AbstractUnifying models have shown that the amount of space used by animals (e.g., activity space, home range) scales allometrically with body mass for terrestrial taxa; however, such relationships are far less clear for marine species. We compiled movement data from 1,596 individuals across 79 taxa collected using a continental passive acoustic telemetry network of acoustic receivers to assess allometric scaling of activity space. We found that ectothermic marine taxa do exhibit allometric scaling for activity space, with an overall scaling exponent of 0.64. However, body mass alone explained only 35% of the variation, with the remaining variation best explained by trophic position for teleosts and latitude for sharks, rays, and marine reptiles. Taxon-specific allometric relationships highlighted weaker scaling exponents among teleost fish species (0.07) than sharks (0.96), rays (0.55), and marine reptiles (0.57). The allometric scaling relationship and scaling exponents for the marine taxonomic groups examined were lower than those reported from studies that had collated both marine and terrestrial species data derived using various tracking methods. We propose that these disparities arise because previous work integrated summarized data across many studies that used differing methods for collecting and quantifying activity space, introducing considerable uncertainty into slope estimates. Our findings highlight the benefit of using large-scale, coordinated animal biotelemetry networks to address cross-taxa evolutionary and ecological questions.

Growth portfolios buffer climate-linked environmental change in marine systems.

Large-scale, climate-induced synchrony in the productivity of fish populations is becoming more pronounced in the world's oceans. As synchrony increases, a population's "portfolio" of responses can be diminished, in turn reducing its resilience to strong perturbation. Here we argue that the costs and benefits of trait synchronization, such as the expression of growth rate, are context dependent. Contrary to prevailing views, synchrony among individuals could actually be beneficial for populations if growth synchrony increases during favorable conditions, and then declines under poor conditions when a broader portfolio of responses could be useful. Importantly, growth synchrony among individuals within populations has seldom been measured, despite well-documented evidence of synchrony across populations. Here, we used century-scale time series of annual otolith growth to test for changes in growth synchronization among individuals within multiple populations of a marine keystone species (Atlantic cod, Gadus morhua). On the basis of 74,662 annual growth increments recorded in 13,749 otoliths, we detected a rising conformity in long-term growth rates within five northeast Atlantic cod populations in response to both favorable growth conditions and a large-scale, multidecadal mode of climate variability similar to the East Atlantic Pattern. The within-population synchrony was distinct from the across-population synchrony commonly reported for large-scale environmental drivers. Climate-linked, among-individual growth synchrony was also identified in other Northeast Atlantic pelagic, deep-sea and bivalve species. We hypothesize that growth synchrony in good years and growth asynchrony in poorer years reflects adaptive trait optimization and bet hedging, respectively, that could confer an unexpected, but pervasive and stabilizing, impact on marine population productivity in response to large-scale environmental change.

Diving into the vertical dimension of elasmobranch movement ecology.

Knowledge of the three-dimensional movement patterns of elasmobranchs is vital to understand their ecological roles and exposure to anthropogenic pressures. To date, comparative studies among species at global scales have mostly focused on horizontal movements. Our study addresses the knowledge gap of vertical movements by compiling the first global synthesis of vertical habitat use by elasmobranchs from data obtained by deployment of 989 biotelemetry tags on 38 elasmobranch species. Elasmobranchs displayed high intra- and interspecific variability in vertical movement patterns. Substantial vertical overlap was observed for many epipelagic elasmobranchs, indicating an increased likelihood to display spatial overlap, biologically interact, and share similar risk to anthropogenic threats that vary on a vertical gradient. We highlight the critical next steps toward incorporating vertical movement into global management and monitoring strategies for elasmobranchs, emphasizing the need to address geographic and taxonomic biases in deployments and to concurrently consider both horizontal and vertical movements.

Effects of human footprint and biophysical factors on the body-size structure of fished marine species.

Marine fisheries in coastal ecosystems in many areas of the world have historically removed large-bodied individuals, potentially impairing ecosystem functioning and the long-term sustainability of fish populations. Reporting on size-based indicators that link to food-web structure can contribute to ecosystem-based management, but the application of these indicators over large (cross-ecosystem) geographical scales has been limited to either fisheries-dependent catch data or diver-based methods restricted to shallow waters (<20 m) that can misrepresent the abundance of large-bodied fished species. We obtained data on the body-size structure of 82 recreationally or commercially targeted marine demersal teleosts from 2904 deployments of baited remote underwater stereo-video (stereo-BRUV). Sampling was at up to 50 m depth and covered approximately 10,000 km of the continental shelf of Australia. Seascape relief, water depth, and human gravity (i.e., a proxy of human impacts) were the strongest predictors of the probability of occurrence of large fishes and the abundance of fishes above the minimum legal size of capture. No-take marine reserves had a positive effect on the abundance of fishes above legal size, although the effect varied across species groups. In contrast, sublegal fishes were best predicted by gradients in sea surface temperature (mean and variance). In areas of low human impact, large fishes were about three times more likely to be encountered and fishes of legal size were approximately five times more abundant. For conspicuous species groups with contrasting habitat, environmental, and biogeographic affinities, abundance of legal-size fishes typically declined as human impact increased. Our large-scale quantitative analyses highlight the combined importance of seascape complexity, regions with low human footprint, and no-take marine reserves in protecting large-bodied fishes across a broad range of species and ecosystem configurations.

Las pesquerías marinas de los ecosistemas costeros en muchas áreas del mundo históricamente han removido a individuos de gran tamaño, potencialmente perjudicando el funcionamiento ambiental y la sostenibilidad a largo plazo de las poblaciones de peces. Los reportes sobre los indicadores basados en el tamaño que se vinculan con la estructura de la red alimenticia pueden contribuir al manejo basado en el ecosistema, aunque la aplicación de estos indicadores a grandes (inter-ecosistemas) escalas geográficas ha estado limitada a datos de captura dependientes de las pesquerías o métodos basados en el buceo restringidos a aguas someras (<20 m), lo cual puede representar erróneamente la abundancia de peces de gran tamaño capturados para la pesca. Obtuvimos los datos de la estructura del tamaño corporal de 82 teleósteos marinos demersales focalizados por razones recreativas o comerciales tomados de 2,904 despliegues de video estéreo subacuático remoto con cebo (stereo-BRUV, en inglés). El muestreo se realizó hasta los 50 metros de profundidad y abarcó aproximadamente 10,000 km del talud continental de Australia. El relieve marino, la profundidad del agua y la gravedad humana (es decir, un indicador de los impactos humanos) fueron los pronosticadores más sólidos de la probabilidad de incidencia de los peces de gran tamaño y de la abundancia de peces por encima del tamaño legal mínimo de captura. Las reservas marinas de protección total tienen un efecto positivo sobre la abundancia de los peces que están por encima del tamaño legal, aunque el efecto varió según el grupo de especies. Como contraste, los peces de tamaño sublegal fueron pronosticados de mejor manera usando gradientes de la temperatura de la superficie marina (media y varianza). En las áreas con un impacto humano reducido, los peces de gran tamaño corporal tenían hasta tres veces mayor probabilidad de aparecer y los peces de tamaño legal eran aproximadamente cinco veces más abundantes. Para los grupos de especies conspicuas con afinidades contrastantes de hábitat, ambiente y biogeografía, la abundancia de peces de tamaño legal normalmente declinó conforme aumentó el impacto humano. Nuestros análisis cuantitativos a gran escala resaltan la importancia conjunta que tienen la complejidad marina, las regiones con una huella humana reducida y las reservas marinas de protección total para la protección de los peces de gran tamaño corporal en una extensa gama de especies y configuraciones ecosistémicas. Efectos de la Huella Humana y los Factores Biofísicos sobre la Estructura del Tamaño Corporal de Especies Marinas Capturadas para la Pesca.

Individual haplotyping of whale sharks from seawater environmental DNA.

Population genetic data can provide valuable information on the demography of a species. For rare and elusive marine megafauna, samples for generating the data are traditionally obtained from tissue biopsies, which can be logistically difficult and expensive to collect and require invasive sampling techniques. Analysis of environmental DNA (eDNA) offers an alternative, minimally invasive approach to provide important genetic information. Although eDNA approaches have been studied extensively for species detection and biodiversity monitoring in metabarcoding studies, the potential for the technique to address population-level questions remains largely unexplored. Here, we applied "eDNA haplotyping" to obtain estimates of the intraspecific genetic diversity of a whale shark (Rhincodon typus) aggregation at Ningaloo reef, Australia. Over 2 weeks, we collected seawater samples directly behind individual sharks prior to taking a tissue biopsy sample from the same animal. Our data showed a 100% match between mtDNA sequences recovered in the eDNA and tissue sample for all 28 individuals sampled. In the seawater samples, >97% of all reads were assigned to six dominant haplotypes, and a clear dominant signal (~99% of sample reads) was recovered in each sample. Our study demonstrates accurate individual-level haplotyping from seawater eDNA. When DNA from one individual clearly dominates each eDNA sample, it provides many of the same opportunities for population genetic analyses as a tissue sample, potentially removing the need for tissue sampling. Our results show that eDNA approaches for population-level analyses have the potential to supply critical demographic data for the conservation and management of marine megafauna.

The power of national acoustic tracking networks to assess the impacts of human activity on marine organisms during the COVID-19 pandemic.

COVID-19 restrictions have led to an unprecedented global hiatus in anthropogenic activities, providing a unique opportunity to assess human impact on biological systems. Here, we describe how a national network of acoustic tracking receivers can be leveraged to assess the effects of human activity on animal movement and space use during such global disruptions. We outline variation in restrictions on human activity across Australian states and describe four mechanisms affecting human interactions with the marine environment: 1) reduction in economy and trade changing shipping traffic; 2) changes in export markets affecting commercial fisheries; 3) alterations in recreational activities; and 4) decline in tourism. We develop a roadmap for the analysis of acoustic tracking data across various scales using Australia's national Integrated Marine Observing System (IMOS) Animal Tracking Facility as a case study. We illustrate the benefit of sustained observing systems and monitoring programs by assessing how a 51-day break in white shark (Carcharodon carcharias) cage-diving tourism due to COVID-19 restrictions affected the behaviour and space use of two resident species. This cessation of tourism activities represents the longest break since cage-diving vessels started day trips in this area in 2007. Long-term monitoring of the local environment reveals that the activity space of yellowtail kingfish (Seriola lalandi) was reduced when cage-diving boats were absent compared to periods following standard tourism operations. However, white shark residency and movements were not affected. Our roadmap is globally applicable and will assist researchers in designing studies to assess how anthropogenic activities can impact animal movement and distributions during regional, short-term through to major, unexpected disruptions like the COVID-19 pandemic.

A large-scale experiment finds no evidence that a seismic survey impacts a demersal fish fauna.

Seismic surveys are used to locate oil and gas reserves below the seabed and can be a major source of noise in marine environments. Their effects on commercial fisheries are a subject of debate, with experimental studies often producing results that are difficult to interpret. We overcame these issues in a large-scale experiment that quantified the impacts of exposure to a commercial seismic source on an assemblage of tropical demersal fishes targeted by commercial fisheries on the North West Shelf of Western Australia. We show that there were no short-term (days) or long-term (months) effects of exposure on the composition, abundance, size structure, behavior, or movement of this fauna. These multiple lines of evidence suggest that seismic surveys have little impact on demersal fishes in this environment.

Natural nutrient subsidies alter demographic rates in a functionally important coral-reef fish.

By improving resource quality, cross-ecosystem nutrient subsidies may boost demographic rates of consumers in recipient ecosystems, which in turn can affect population and community dynamics. However, empirical studies on how nutrient subsidies simultaneously affect multiple demographic rates are lacking, in part because humans have disrupted the majority of these natural flows. Here, we compare the demographics of a sex-changing parrotfish (Chlorurus sordidus) between reefs where cross-ecosystem nutrients provided by seabirds are available versus nearby reefs where invasive, predatory rats have removed seabird populations. For this functionally important species, we found evidence for a trade-off between investing in growth and fecundity, with parrotfish around rat-free islands with many seabirds exhibiting 35% faster growth, but 21% lower size-based fecundity, than those around rat-infested islands with few seabirds. Although there were no concurrent differences in population-level density or biomass, overall mean body size was 16% larger around rat-free islands. Because the functional significance of parrotfish as grazers and bioeroders increases non-linearly with size, the increased growth rates and body sizes around rat-free islands likely contributes to higher ecosystem function on coral reefs that receive natural nutrient subsidies. More broadly, these results demonstrate additional benefits, and potential trade-offs, of restoring natural nutrient pathways for recipient ecosystems.

Isolated reefs support stable fish communities with high abundances of regionally fished species.

Anthropogenic impacts at isolated and inaccessible reefs are often minimal, offering rare opportunities to observe fish assemblages in a relatively undisturbed state. The remote Rowley Shoals are regarded as one of the healthiest reef systems in the Indian Ocean with demonstrated resilience to natural disturbance, no permanent human population nearby, low visitation rates, and large protected areas where fishing prohibitions are enforced. We used baited remote underwater video systems (BRUVS) to quantify fish assemblages and the relative abundance of regionally fished species within the lagoon, on the slope and in the mesophotic habitat at the Rowley Shoals at three times spanning 14 years and compared abundances of regionally fished species and the length distributions of predatory species to other isolated reefs in the northeast Indian Ocean. Fish assemblage composition and the relative abundance of regionally fished species were remarkably stable through time. We recorded high abundances of regionally fished species relative to other isolated reefs, including globally threatened humphead Maori wrasse (Cheilinus undulatus) and bumphead parrotfish (Bolbometopon muricatum). Length distributions of fish differed among habitats at the Rowley Shoals, suggesting differences in ontogenetic shifts among species. The Cocos (Keeling) Islands typically had larger-bodied predatory species than at the Rowley Shoals. Differences in geomorphology, lagoonal habitats, and fishing history likely contribute to the differences among remote reefs. Rowley Shoals is a rare example of a reef system demonstrating ecological stability in reef fish assemblages during a time of unprecedented degradation of coral reefs.

Increased connectivity and depth improve the effectiveness of marine reserves.

Marine reserves are a key tool for the conservation of marine biodiversity, yet only ~2.5% of the world's oceans are protected. The integration of marine reserves into connected networks representing all habitats has been encouraged by international agreements, yet the benefits of this design has not been tested empirically. Australia has one of the largest systems of marine reserves, providing a rare opportunity to assess how connectivity influences conservation success. An Australia-wide dataset was collected using baited remote underwater video systems deployed across a depth range from 0 to 100 m to assess the effectiveness of marine reserves for protecting teleosts subject to commercial and recreational fishing. A meta-analytical comparison of 73 fished species within 91 marine reserves found that, on average, marine reserves had 28% greater abundance and 53% greater biomass of fished species compared to adjacent areas open to fishing. However, benefits of protection were not observed across all reserves (heterogeneity), so full subsets generalized additive modelling was used to consider factors that influence marine reserve effectiveness, including distance-based and ecological metrics of connectivity among reserves. Our results suggest that increased connectivity and depth improve the aforementioned marine reserve benefits and that these factors should be considered to optimize such benefits over time. We provide important guidance on factors to consider when implementing marine reserves for the purpose of increasing the abundance and size of fished species, given the expected increase in coverage globally. We show that marine reserves that are highly protected (no-take) and designed to optimize connectivity, size and depth range can provide an effective conservation strategy for fished species in temperate and tropical waters within an overarching marine biodiversity conservation framework.

Moray eels are more common on coral reefs subject to higher human pressure in the greater Caribbean.

Proximity and size of the nearest market ('market gravity') have been shown to have strong negative effects on coral reef fish communities that can be mitigated by the establishment of closed areas. However, moray eels are functionally unique predators that are generally not subject to targeted fishing and should therefore not directly be affected by these factors. We used baited remote underwater video systems to investigate associations between morays and anthropogenic, habitat, and ecological factors in the Caribbean region. Market gravity had a positive effect on morays, while the opposite pattern was observed in a predator group subject to exploitation (sharks). Environmental DNA analyses corroborated the positive effect of market gravity on morays. We hypothesize that the observed pattern could be the indirect result of the depletion of moray competitors and predators near humans.

The soundscape of the Anthropocene ocean.

Oceans have become substantially noisier since the Industrial Revolution. Shipping, resource exploration, and infrastructure development have increased the anthrophony (sounds generated by human activities), whereas the biophony (sounds of biological origin) has been reduced by hunting, fishing, and habitat degradation. Climate change is affecting geophony (abiotic, natural sounds). Existing evidence shows that anthrophony affects marine animals at multiple levels, including their behavior, physiology, and, in extreme cases, survival. This should prompt management actions to deploy existing solutions to reduce noise levels in the ocean, thereby allowing marine animals to reestablish their use of ocean sound as a central ecological trait in a healthy ocean.