Divergent responses of pelagic and benthic fish body-size structure to remoteness and protection from humans.

Animal body-size variation influences multiple processes in marine ecosystems, but habitat heterogeneity has prevented a comprehensive assessment of size across pelagic (midwater) and benthic (seabed) systems along anthropic gradients. In this work, we derive fish size indicators from 17,411 stereo baited-video deployments to test for differences between pelagic and benthic responses to remoteness from human pressures and effectiveness of marine protected areas (MPAs). From records of 823,849 individual fish, we report divergent responses between systems, with pelagic size structure more profoundly eroded near human markets than benthic size structure, signifying greater vulnerability of pelagic systems to human pressure. Effective protection of benthic size structure can be achieved through MPAs placed near markets, thereby contributing to benthic habitat restoration and the recovery of associated fishes. By contrast, recovery of the world's largest and most endangered fishes in pelagic systems requires the creation of highly protected areas in remote locations, including on the High Seas, where protection efforts lag.

Changes in illegal fishing dynamics in a large-scale MPA during COVID-19.

Global socio-ecological shocks, such as the COVID-19 pandemic, can threaten progress in protecting vulnerable marine environments by altering behaviour of resource users1. When government priorities shift from environmental protection towards safeguarding human populations, control of illegal activity in protected areas can alter. Resulting increases in illegal fishing in large-scale marine protected areas (MPAs) are of particular concern as they contain a large proportion of marine protected area globally2. Here, we report on average 19 times as many suspected illegal fishing vessels per month in 2022 (n = 19) compared with 2010 to 2020 (n = 1) in an Indian Ocean MPA. Although illegal fishing has been a pervasive problem, the current spike in Indian vessels targeting a broad trophic diversity of reef-associated species is of particular concern and we suggest such changes in illegal activity in MPAs globally may persist over long timescales unless management is broad and adaptive to individual context. When considering potential solutions, widespread adoption of technology, such as remote surveillance of vessels, can mitigate illegal activities but remains unfeasible for many MPAs globally due to financial and political barriers. Instead, we suggest broader approaches, including a renewed focus on regional approaches to combating illegal fishing, formal bilateral agreements between competent authorities in relevant countries and an increase in community-based work.

Contrasting ecological information content in whaling archives with modern cetacean surveys for conservation planning and identification of historical distribution changes.

Many species are restricted to a marginal or suboptimal fraction of their historical range due to anthropogenic impacts, making it hard to interpret their ecological preferences from modern-day data alone. However, inferring past ecological states is limited by the availability of robust data and biases in historical archives, posing a challenge for policy makers . To highlight how historical records can be used to understand the ecological requirements of threatened species and inform conservation, we investigated sperm whale (Physeter macrocephalus) distribution in the Western Indian Ocean. We assessed differences in information content and habitat suitability predictions based on whale occurrence data from Yankee whaling logs (1792-1912) and from modern cetacean surveys (1995-2020). We built maximum entropy habitat suitability models containing static (bathymetry-derived) variables to compare models comprising historical-only and modern-only data. Using both historical and modern habitat suitability predictions  we assessed marine protected area (MPA) placement by contrasting suitability in- and outside MPAs. The historical model predicted high habitat suitability in shelf and coastal regions near continents and islands, whereas the modern model predicted a less coastal distribution with high habitat suitability more restricted to areas of steep topography. The proportion of high habitat suitability inside versus outside MPAs was higher when applying the historical predictions than the modern predictions, suggesting that different marine spatial planning optimums can be reached from either data sources. Moreover, differences in relative habitat suitability predictions between eras were consistent with the historical depletion of sperm whales from coastal regions, which were easily accessed and targeted by whalers, resulting in a modern distribution limited more to steep continental margins and remote oceanic ridges. The use of historical data can provide important new insights and, through cautious interpretation, inform conservation planning and policy, for example, by identifying refugee species and regions of anticipated population recovery.

Contrastes del contenido de información ecológica entre los archivos de la caza de ballenas y los censos actuales de cetáceos para la planeación de la conservación y la identificación de cambios en la distribución histórica Resumen Muchas especies están restringidas a una fracción marginal o subóptima de su área de distribución histórica debido a impactos antropogénicos. Esto dificulta interpretar sus preferencias ecológicas con sólo usar los datos actuales. Sin embargo, la inferencia de estados ecológicos pasados está limitada a la disponibilidad de datos sólidos y a los sesgos de los archivos históricos, lo que plantea un reto para la conservación y los responsables de las políticas. Analizamos la distribución del cachalote (Physeter macrocephalus) en el Océano Índico occidental para resaltar cómo pueden utilizarse los registros históricos para comprender los requisitos ecológicos de las especies amenazadas y direccionar su conservación. Evaluamos las diferencias en el contenido de la información y las predicciones de idoneidad del hábitat basadas en los datos de presencia de ballenas de los registros balleneros Yanquis (1792-1912) y de los estudios actuales sobre cetáceos (1995-2020). Construimos modelos de idoneidad de hábitat con máxima entropía que incluían variables estáticas (derivadas de la batimetría) para comparar los modelos que abarcan datos históricos y actuales. Evaluamos la ubicación de las áreas marinas protegidas (AMP) contrastando las predicciones dentro y fuera de ellas con los modelos históricos y actuales de la idoneidad del hábitat. El modelo histórico predijo una alta idoneidad del hábitat en las regiones costeras y de la plataforma continental cercanas a los continentes e islas, mientras que el modelo moderno predijo una distribución menos costera con una alta idoneidad del hábitat más restringida a las zonas de topografía escarpada. La proporción de hábitats de alta idoneidad dentro y fuera de las AMP fue mayor con la aplicación de las predicciones históricas que con la de las modernas, lo que sugiere que se pueden alcanzar diferentes niveles óptimos de ordenación del espacio marino a partir de ambas fuentes de datos. Además, las diferencias entre los periodos en las predicciones relacionadas con la idoneidad del hábitat fueron coherentes con la reducción histórica de los cachalotes en las regiones costeras, las cuales eran fácilmente accesibles para los balleneros, lo que resultó en una distribución actual más limitada a los márgenes continentales escarpados y a las crestas oceánicas remotas. El uso de datos históricos puede aportar nuevos e importantes conocimientos e informar, mediante una interpretación prudente, a la planificación y la política de conservación; por ejemplo, con la identificación de especies refugiadas y regiones de recuperación poblacional.

How many replicates to accurately estimate fish biodiversity using environmental DNA on coral reefs?

Quantifying fish species diversity in rich tropical marine environments remains challenging. Environmental DNA (eDNA) metabarcoding is a promising tool to face this challenge through the filtering, amplification, and sequencing of DNA traces from water samples. However, because eDNA concentration is low in marine environments, the reliability of eDNA to detect species diversity can be limited. Using an eDNA metabarcoding approach to identify fish Molecular Taxonomic Units (MOTUs) with a single 12S marker, we aimed to assess how the number of sampling replicates and filtered water volume affect biodiversity estimates. We used a paired sampling design of 30 L per replicate on 68 reef transects from 8 sites in 3 tropical regions. We quantified local and regional sampling variability by comparing MOTU richness, compositional turnover, and compositional nestedness. We found strong turnover of MOTUs between replicated pairs of samples undertaken in the same location, time, and conditions. Paired samples contained non-overlapping assemblages rather than subsets of one another. As a result, non-saturated localized diversity accumulation curves suggest that even 6 replicates (180 L) in the same location can underestimate local diversity (for an area <1 km). However, sampling regional diversity using ~25 replicates in variable locations (often covering 10 s of km) often saturated biodiversity accumulation curves. Our results demonstrate variability of diversity estimates possibly arising from heterogeneous distribution of eDNA in seawater, highly skewed frequencies of eDNA traces per MOTU, in addition to variability in eDNA processing. This high compositional variability has consequences for using eDNA to monitor temporal and spatial biodiversity changes in local assemblages. Avoiding false-negative detections in future biomonitoring efforts requires increasing replicates or sampled water volume to better inform management of marine biodiversity using eDNA.

Detection of the elusive Dwarf sperm whale (Kogia sima) using environmental DNA at Malpelo island (Eastern Pacific, Colombia).

Monitoring large marine mammals is challenging due to their low abundances in general, an ability to move over large distances and wide geographical range sizes.The distribution of the pygmy (Kogia breviceps) and dwarf (Kogia sima) sperm whales is informed by relatively rare sightings, which does not permit accurate estimates of their distribution ranges. Hence, their conservation status has long remained Data Deficient (DD) in the Red list of the International Union for Conservation of Nature (IUCN), which prevent appropriate conservation measures.Environmental DNA (eDNA) metabarcoding uses DNA traces left by organisms in their environments to detect the presence of targeted taxon, and is here proved to be useful to increase our knowledge on the distribution of rare but emblematic megafauna.Retrieving eDNA from filtered surface water provides the first detection of the Dwarf sperm whale (Kogia sima) around the remote Malpelo island (Colombia).Environmental DNA collected during oceanic missions can generate better knowledge on rare but emblematic animals even in regions that are generally well sampled for other taxa.

Improved bathymetry leads to >4000 new seamount predictions in the global ocean - but beware of phantom seamounts!

Seamounts are important marine habitats that are hotspots of species diversity. Relatively shallow peaks, increased productivity and offshore locations make seamounts vulnerable to human impact and difficult to protect. Present estimates of seamount numbers vary from anywhere between 10,000 to more than 60,000. Seamount locations can be estimated by extracting large, cone-like features from bathymetry grids (based on criteria of size and shape). These predicted seamounts are a useful reference for marine researchers and can help direct exploratory surveys. However, these predictions are dependent on the quality of the surveys underpinning the bathymetry. Historically, quality has been patchy, but is improving as mapping efforts step up towards the target of complete seabed coverage by 2030. This study presents an update of seamount predictions based on SRTM30 PLUS global bathymetry version 11 and examines a potential source of error in these predictions. This update was prompted by a seamount survey in the British Indian Ocean Territory in 2016, where locations of two putative seamounts were visited. These 'seamounts' were targeted based on previous predictions, but these features were not detected during echosounder surveys. An examination of UK hydrographic office navigational (Admiralty) charts for the area showed that the summits of these putative features had soundings reporting 'no bottom detected at this depth' where 'this depth' was similar to the seabed reported from the bathymetry grids: we suspect that these features likely resulted from an initial misreading of the charts. We show that 15 'phantom seamount' features, derived from a misinterpretation of no bottom sounding data, persist in current global bathymetry grids and updated seamount predictions. Overall, we predict 37,889 seamounts, an increase of 4437 from the previous predictions derived from an older global bathymetry grid (SRTM30 PLUS v6). This increase is due to greater detail in newer bathymetry grids as acoustic mapping of the seabed expands. The new seamount predictions are available at https://doi.pangaea.de/10.1594/PANGAEA.921688.

Climate oscillation and the invasion of alien species influence the oceanic distribution of seabirds.

Spatial and temporal distribution of seabird transiting and foraging at sea is an important consideration for marine conservation planning. Using at-sea observations of seabirds (n = 317), collected during the breeding season from 2012 to 2016, we built boosted regression tree (BRT) models to identify relationships between numerically dominant seabird species (red-footed booby, brown noddy, white tern, and wedge-tailed shearwater), geomorphology, oceanographic variability, and climate oscillation in the Chagos Archipelago. We documented positive relationships between red-footed booby and wedge-tailed shearwater abundance with the strength in the Indian Ocean Dipole, as represented by the Dipole Mode Index (6.7% and 23.7% contribution, respectively). The abundance of red-footed boobies, brown noddies, and white terns declined abruptly with greater distance to island (17.6%, 34.1%, and 41.1% contribution, respectively). We further quantified the effects of proximity to rat-free and rat-invaded islands on seabird distribution at sea and identified breaking point distribution thresholds. We detected areas of increased abundance at sea and habitat use-age under a scenario where rats are eradicated from invaded nearby islands and recolonized by seabirds. Following rat eradication, abundance at sea of red-footed booby, brown noddy, and white terns increased by 14%, 17%, and 3%, respectively, with no important increase detected for shearwaters. Our results have implication for seabird conservation and island restoration. Climate oscillations may cause shifts in seabird distribution, possibly through changes in regional productivity and prey distribution. Invasive species eradications and subsequent island recolonization can lead to greater access for seabirds to areas at sea, due to increased foraging or transiting through, potentially leading to distribution gains and increased competition. Our approach predicting distribution after successful eradications enables anticipatory threat mitigation in these areas, minimizing competition between colonies and thereby maximizing the risk of success and the conservation impact of eradication programs.

Correction: Remote reefs and seamounts are the last refuges for marine predators across the Indo-Pacific.

[This corrects the article DOI: 10.1371/journal.pbio.3000366.].

Remote reefs and seamounts are the last refuges for marine predators across the Indo-Pacific.

Since the 1950s, industrial fisheries have expanded globally, as fishing vessels are required to travel further afield for fishing opportunities. Technological advancements and fishery subsidies have granted ever-increasing access to populations of sharks, tunas, billfishes, and other predators. Wilderness refuges, defined here as areas beyond the detectable range of human influence, are therefore increasingly rare. In order to achieve marine resources sustainability, large no-take marine protected areas (MPAs) with pelagic components are being implemented. However, such conservation efforts require knowledge of the critical habitats for predators, both across shallow reefs and the deeper ocean. Here, we fill this gap in knowledge across the Indo-Pacific by using 1,041 midwater baited videos to survey sharks and other pelagic predators such as rainbow runner (Elagatis bipinnulata), mahi-mahi (Coryphaena hippurus), and black marlin (Istiompax indica). We modeled three key predator community attributes: vertebrate species richness, mean maximum body size, and shark abundance as a function of geomorphology, environmental conditions, and human pressures. All attributes were primarily driven by geomorphology (35%-62% variance explained) and environmental conditions (14%-49%). While human pressures had no influence on species richness, both body size and shark abundance responded strongly to distance to human markets (12%-20%). Refuges were identified at more than 1,250 km from human markets for body size and for shark abundance. These refuges were identified as remote and shallow seabed features, such as seamounts, submerged banks, and reefs. Worryingly, hotpots of large individuals and of shark abundance are presently under-represented within no-take MPAs that aim to effectively protect marine predators, such as the British Indian Ocean Territory. Population recovery of predators is unlikely to occur without strategic placement and effective enforcement of large no-take MPAs in both coastal and remote locations.

Isolation and no-entry marine reserves mitigate anthropogenic impacts on grey reef shark behavior.

Reef sharks are vulnerable predators experiencing severe population declines mainly due to overexploitation. However, beyond direct exploitation, human activities can produce indirect or sub-lethal effects such as behavioral alterations. Such alterations are well known for terrestrial fauna but poorly documented for marine species. Using an extensive sampling of 367 stereo baited underwater videos systems, we show modifications in grey reef shark (Carcharhinus amblyrhynchos) occurrence and feeding behavior along a marked gradient of isolation from humans across the New Caledonian archipelago (South-Western Pacific). The probability of occurrence decreased by 68.9% between wilderness areas (more than 25 hours travel time from the capital city) and impacted areas while the few individuals occurring in impacted areas exhibited cautious behavior. We also show that only large no-entry reserves (above 150 km²) can protect the behavior of grey reef sharks found in the wilderness. Influencing the fitness, human linked behavioral alterations should be taken into account for management strategies to ensure the persistence of populations.

Correction: Drivers of abundance and spatial distribution of reef-associated sharks in an isolated atoll reef system.

[This corrects the article DOI: 10.1371/journal.pone.0177374.].

Drivers of abundance and spatial distribution of reef-associated sharks in an isolated atoll reef system.

We investigated drivers of reef shark demography across a large and isolated marine protected area, the British Indian Ocean Territory Marine Reserve, using stereo baited remote underwater video systems. We modelled shark abundance against biotic and abiotic variables at 35 sites across the reserve and found that the biomass of low trophic order fish (specifically planktivores) had the greatest effect on shark abundance, although models also included habitat variables (depth, coral cover and site type). There was significant variation in the composition of the shark assemblage at different atolls within the reserve. In particular, the deepest habitat sampled (a seamount at 70-80m visited for the first time in this study) recorded large numbers of scalloped hammerhead sharks (Sphyrna lewini) not observed elsewhere. Size structure of the most abundant and common species, grey reef sharks (Carcharhinus amblyrhynchos), varied with location. Individuals at an isolated bank were 30% smaller than those at the main atolls, with size structure significantly biased towards the size range for young of year (YOY). The 18 individuals judged to be YOY represented the offspring of between four and six females, so, whilst inconclusive, these data suggest the possible use of a common pupping site by grey reef sharks. The importance of low trophic order fish biomass (i.e. potential prey) in predicting spatial variation in shark abundance is consistent with other studies both in marine and terrestrial systems which suggest that prey availability may be a more important predictor of predator distribution than habitat suitability. This result supports the need for ecosystem level rather than species-specific conservation measures to support shark recovery. The observed spatial partitioning amongst sites for species and life-stages also implies the need to include a diversity of habitats and reef types within a protected area for adequate protection of reef-associated shark assemblages.

Sampling mobile oceanic fishes and sharks: implications for fisheries and conservation planning.

Tuna, billfish, and oceanic sharks [hereafter referred to as 'mobile oceanic fishes and sharks' (MOFS)] are characterised by conservative life-history strategies and highly migratory behaviour across large, transnational ranges. Intense exploitation over the past 65 years by a rapidly expanding high-seas fishing fleet has left many populations depleted, with consequences at the ecosystem level due to top-down control and trophic cascades. Despite increases in both CITES and IUCN Red Listings, the demographic trajectories of oceanic sharks and billfish are poorly quantified and resolved at geographic and population levels. Amongst MOFS trajectories, those of tunas are generally considered better understood, yet several populations remain either overfished or of unknown status. MOFS population trends and declines therefore remain contentious, partly due to challenges in deriving accurate abundance and biomass indices. Two major management strategies are currently recognised to address conservation issues surrounding MOFS: (i) internationally ratified legal frameworks and their associated regional fisheries management organisations (RFMOs); and (ii) spatio-temporal fishery closures, including no-take marine protected areas (MPAs). In this context, we first review fishery-dependent studies relying on data derived from catch records and from material accessible through fishing extraction, under the umbrella of RFMO-administrated management. Challenges in interpreting catch statistics notwithstanding, we find that fishery-dependent studies have enhanced the accuracy of biomass indices and the management strategies they inform, by addressing biases in reporting and non-random effort, and predicting drivers of spatial variability across meso- and oceanic scales in order to inform stock assessments. By contrast and motivated by the increase in global MPA coverage restricting extractive activities, we then detail ways in which fishery-independent methods are increasingly improving and steering management by exploring facets of MOFS ecology thus far poorly grasped. Advances in telemetry are increasingly used to explore ontogenic and seasonal movements, and provide means to consider MOFS migration corridors and residency patterns. The characterisation of trophic relationships and prey distribution through biochemical analysis and hydro-acoustics surveys has enabled the tracking of dietary shifts and mapping of high-quality foraging grounds. We conclude that while a scientific framework is available to inform initial design and subsequent implementation of MPAs, there is a shortage in the capacity to answer basic but critical questions about MOFS ecology (who, when, where?) required to track populations non-extractively, thereby presenting a barrier to assessing empirically the performance of MPA-based management for MOFS. This sampling gap is exacerbated by the increased establishment of large (>10000 km2 ) and very large MPAs (VLMPAs, >100000 km2 ) - great expanses of ocean lacking effective monitoring strategies and survey regimes appropriate to those scales. To address this shortcoming, we demonstrate the use of a non-extractive protocol to measure MOFS population recovery and MPA efficiency. We further identify technological avenues for monitoring at the VLMPA scale, through the use of spotter planes, drones, satellite technology, and horizontal acoustics, and highlight their relevance to the ecosystem-based framework of MOFS management.

Topographic determinants of mobile vertebrate predator hotspots: current knowledge and future directions.

Despite being identified as a driver of mobile predator aggregations (hotspots) in both marine and terrestrial environments, topographic complexity has long remained a challenging concept for scientists to visualise and a difficult parameter to estimate. It is only with the advent of high-speed computers and the recent popularisation of geographical information systems (GIS) that terrain attributes have begun to be quantitatively measured in three-dimensional space and related to wildlife dynamics, making the well-established field of geomorphometry (or 'digital terrain modelling') a discipline of growing appeal to biologists. Although a diverse array of numerical metrics is now available to describe the shape, geometry and physical properties of natural habitats, few of these are known to, or adequately used by, ecologists. In this review, we examine the nature and usage of 56 geomorphometrics extracted from the ecological modelling literature over a period of 32 years (1979-2011). We show that, in studies of mobile predators, numerous topographic variables have largely been overlooked in favour of single basic metrics that do not, on their own, fully capture the complexity of continuous landscapes. Based on a simulation approach, we assess the redundancy and correlation structure of these metrics and demonstrate that a majority are highly collinear. We highlight a suite of 7-8 complementary metrics which best explain topographic patterns across a bathymetric grid of the west Australian seafloor, and contend that field and analytical protocols should prioritise variables of these types, particularly when the responses of predator populations to physical habitat features are of interest. We suggest that prominent structures such as canyons, seamounts or mountain chains can serve as useful proxies for predator hotspots, especially in remote locations where access to high-resolution biological data is often limited.

Does presence of a mid-ocean ridge enhance biomass and biodiversity?

In contrast to generally sparse biological communities in open-ocean settings, seamounts and ridges are perceived as areas of elevated productivity and biodiversity capable of supporting commercial fisheries. We investigated the origin of this apparent biological enhancement over a segment of the North Mid-Atlantic Ridge (MAR) using sonar, corers, trawls, traps, and a remotely operated vehicle to survey habitat, biomass, and biodiversity. Satellite remote sensing provided information on flow patterns, thermal fronts, and primary production, while sediment traps measured export flux during 2007-2010. The MAR, 3,704,404 km(2) in area, accounts for 44.7% lower bathyal habitat (800-3500 m depth) in the North Atlantic and is dominated by fine soft sediment substrate (95% of area) on a series of flat terraces with intervening slopes either side of the ridge axis contributing to habitat heterogeneity. The MAR fauna comprises mainly species known from continental margins with no evidence of greater biodiversity. Primary production and export flux over the MAR were not enhanced compared with a nearby reference station over the Porcupine Abyssal Plain. Biomasses of benthic macrofauna and megafauna were similar to global averages at the same depths totalling an estimated 258.9 kt C over the entire lower bathyal north MAR. A hypothetical flat plain at 3500 m depth in place of the MAR would contain 85.6 kt C, implying an increase of 173.3 kt C attributable to the presence of the Ridge. This is approximately equal to 167 kt C of estimated pelagic biomass displaced by the volume of the MAR. There is no enhancement of biological productivity over the MAR; oceanic bathypelagic species are replaced by benthic fauna otherwise unable to survive in the mid ocean. We propose that globally sea floor elevation has no effect on deep sea biomass; pelagic plus benthic biomass is constant within a given surface productivity regime.