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.

Colour change and colour phases in Lethrinidae with insights into ecology.

Colour change is used by a wide range of animals. It is used for intra- and interspecific communication and crypsis, and can occur on morphological and physiological levels. Bony fish employ rapid physiological colour change and display various types of patterns and colouration (colour phases) useful for aposematic and cryptic purposes. Using an existing database of benthic stereo-baited remote underwater video systems from two locations in Western Australia, we tested whether the frequency of colour phases of emperors, Lethrinidae, varied by species. We described colour phases and rapid physiological colour change in 16 species of lethrinids, and related occurrences of colour change to feeding activity and life stages. Dark and light colour phases were observed in nine of the 16 evaluated species of which seven also displayed physiological colour change. Frequency of colour phases varied between species, suggesting that the display of different dark patterns may be especially important for certain species. Both juveniles and adults showed the ability to change between different colour patterns. The change into a mottled pattern mainly occurred while feeding or when approaching to feed, suggesting that it may be triggered by feeding and the associated decrease in environmental awareness. Colour change is a commonly observed strategy in lethrinids and may have evolved as an adaptation for increased foraging success or to reduce aggression from conspecifics. Physiological colour change allows lethrinids to quickly adapt to various cues from the environment and can therefore be considered a versatile physiological mechanism in this family.

Sharks are the preferred scraping surface for large pelagic fishes: Possible implications for parasite removal and fitness in a changing ocean.

Mutualistic and commensal interactions can have significant positive impacts on animal fitness and survival. However, behavioural interactions between pelagic animals living in offshore oceanic environments are little studied. Parasites can negatively effect the fitness of their hosts by draining resources and diverting energy from growth, reproduction, and other bodily functions. Pelagic fishes are hosts to a diverse array of parasites, however their environment provides few options for removal. Here we provide records of scraping behaviour of several pelagic teleost species, a behaviour that is likely used for parasite removal. These records span three ocean basins and, to the best of our knowledge, include the first records of scraping interactions involving tunas, blue sharks, and mako sharks as well as the first records of intraspecific scraping. We found that scrapers preferred scraping their head, eyes, gill cover, and lateral surfaces, areas where parasites are commonly found and where damage would likely have a substantial impact on fitness. Scraper species varied in their scraping preferences with tunas scraping mostly on the posterior caudal margins of sharks and occasionally conspecifics, while rainbow runner scraped in more varied locations on both sharks and conspecifics. Lengths of scrapers and scrapees were positively correlated and fish scraping on sharks were larger than those scraping on conspecifics, suggesting that risk of predation may be a limiting factor. We show that pelagic teleosts prefer to scrape on sharks rather than conspecifics or other teleosts and suggest that this behaviour may have a positive impact on teleost fitness by reducing parasite loads. The decline of shark populations in the global ocean and the reduction in mean size of many species may limit these interactions, eroding possible fitness benefits associated with this behaviour, and consequently placing more pressure on already highly targeted and vulnerable species.

Offshore platforms as novel ecosystems: A case study from Australia's Northwest Shelf.

The decommissioning of offshore oil and gas platforms typically involves removing some or all of the associated infrastructure and the consequent destruction of the associated marine ecosystem that has developed over decades. There is increasing evidence of the important ecological role played by offshore platforms. Concepts such as novel ecosystems allow stakeholders to consider the ecological role played by each platform in the decommissioning process. This study focused on the Wandoo field in Northwest Australia as a case study for the application of the novel ecosystem concept to the decommissioning of offshore platforms. Stereo-baited remote underwater video systems were used to assess the habitat composition and fish communities at Wandoo, as well as two control sites: a sandy one that resembled the Wandoo site pre-installation, and one characterized by a natural reef as a control for natural hard substrate and vertical relief. We found denser macrobenthos habitat at the Wandoo site than at either of the control sites, which we attributed to the exclusion of seabed trawling around the Wandoo infrastructure. We also found that the demersal and pelagic taxonomic assemblages at Wandoo more closely resemble those at a natural reef than those which would likely have been present pre-installation, but these assemblages are still unique in a regional context. The demersal assemblage is characterized by reef-associated species with higher diversity than those at the sand control and natural reef control sites, with the pelagic community characterized by species associated with oil platforms in other regions. These findings suggest that a novel ecosystem has emerged in the Wandoo field. It is likely that many of the novel qualities of this ecosystem would be lost under decommissioning scenarios that involve partial or complete removal. This study provides an example for classifying offshore platforms as novel ecosystems.

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.

A seafloor habitat map for the Australian continental shelf.

Here we outline the genesis of Seamap Australia, which integrates spatial data of the seabed of Australia's continental shelf (0-200 m depth) from multiple sources to provide a single national map layer of marine habitat. It is underpinned by a hierarchical classification scheme with registered vocabulary, enabling presentation of nationally consistent information at the highest resolution available for any point in space. The Seamap Australia website enables users to delineate particular areas of interest, overlay habitat maps with many other marine data layers, and to directly access the data and metadata underlying the maps they produce. This unique resource represents a step-change in capacity to access and integrate large and diverse marine data holdings and to readily derive information and products to underpin decision making around marine spatial planning and conservation prioritisation, state-of-environment reporting, and research. It is a world first fully integrated national-scale marine mapping and data service.

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.

Modern slavery and the race to fish.

Marine fisheries are in crisis, requiring twice the fishing effort of the 1950s to catch the same quantity of fish, and with many fleets operating beyond economic or ecological sustainability. A possible consequence of diminishing returns in this race to fish is serious labour abuses, including modern slavery, which exploit vulnerable workers to reduce costs. Here, we use the Global Slavery Index (GSI), a national-level indicator, as a proxy for modern slavery and labour abuses in fisheries. GSI estimates and fisheries governance are correlated at the national level among the major fishing countries. Furthermore, countries having documented labour abuses at sea share key features, including higher levels of subsidised distant-water fishing and poor catch reporting. Further research into modern slavery in the fisheries sector is needed to better understand how the issue relates to overfishing and fisheries policy, as well as measures to reduce risk in these labour markets.

Far from home: Distance patterns of global fishing fleets.

Postwar growth of industrial fisheries catch to its peak in 1996 was driven by increasing fleet capacity and geographical expansion. An investigation of the latter, using spatially allocated reconstructed catch data to quantify "mean distance to fishing grounds," found global trends to be dominated by the expansion histories of a small number of distant-water fishing countries. While most countries fished largely in local waters, Taiwan, South Korea, Spain, and China rapidly increased their mean distance to fishing grounds by 2000 to 4000 km between 1950 and 2014. Others, including Japan and the former USSR, expanded in the postwar decades but then retrenched from the mid-1970s, as access to other countries' waters became increasingly restricted with the advent of exclusive economic zones formalized in the 1982 United Nations Convention on the Law of the Sea. Since 1950, heavily subsidized fleets have increased the total fished area from 60% to more than 90% of the world's oceans, doubling the average distance traveled from home ports but catching only one-third of the historical amount per kilometer traveled. Catch per unit area has declined by 22% since the mid-1990s, as fleets approach the limits of geographical expansion. Allowing these trends to continue threatens the bioeconomic sustainability of fisheries globally.

Challenges of transferring models of fish abundance between coral reefs.

Reliable abundance estimates for species are fundamental in ecology, fisheries, and conservation. Consequently, predictive models able to provide reliable estimates for un- or poorly-surveyed locations would prove a valuable tool for management. Based on commonly used environmental and physical predictors, we developed predictive models of total fish abundance and of abundance by fish family for ten representative taxonomic families for the Great Barrier Reef (GBR) using multiple temporal scenarios. We then tested if models developed for the GBR (reference system) could predict fish abundances at Ningaloo Reef (NR; target system), i.e., if these GBR models could be successfully transferred to NR. Models of abundance by fish family resulted in improved performance (e.g., 44.1%  0.05). High spatio-temporal variability of patterns in fish abundance at the family and population levels in both reef systems likely affected the transferability of these models. Inclusion of additional predictors with potential direct effects on abundance, such as local fishing effort or topographic complexity, may improve transferability of fish abundance models. However, observations of these local-scale predictors are often not available, and might thereby hinder studies on model transferability and its usefulness for conservation planning and management.

A boundary current drives synchronous growth of marine fishes across tropical and temperate latitudes.

Entrainment of growth patterns of multiple species to single climatic drivers can lower ecosystem resilience and increase the risk of species extinction during stressful climatic events. However, predictions of the effects of climate change on the productivity and dynamics of marine fishes are hampered by a lack of historical data on growth patterns. We use otolith biochronologies to show that the strength of a boundary current, modulated by the El Niño-Southern Oscillation, accounted for almost half of the shared variance in annual growth patterns of five of six species of tropical and temperate marine fishes across 23° of latitude (3000 km) in Western Australia. Stronger flow during La Niña years drove increased growth of five species, whereas weaker flow during El Niño years reduced growth. Our work is the first to link the growth patterns of multiple fishes with a single oceanographic/climate phenomenon at large spatial scales and across multiple climate zones, habitat types, trophic levels and depth ranges. Extreme La Niña and El Niño events are predicted to occur more frequently in the future and these are likely to have implications for these vulnerable ecosystems, such as a limited capacity of the marine taxa to recover from stressful climatic events.

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.].

The trophic role of a large marine predator, the tiger shark Galeocerdo cuvier.

Tiger sharks were sampled off the western (Ningaloo Reef, Shark Bay) and eastern (the Great Barrier Reef; GBR, Queensland and New South Wales; NSW) coastlines of Australia. Multiple tissues were collected from each shark to investigate the effects of location, size and sex of sharks on δ13C and δ15N stable isotopes among these locations. Isotopic composition of sharks sampled in reef and seagrass habitats (Shark Bay, GBR) reflected seagrass-based food-webs, whereas at Ningaloo Reef analysis revealed a dietary transition between pelagic and seagrass food-webs. In temperate habitats off southern Queensland and NSW coasts, shark diets relied on pelagic food-webs. Tiger sharks occupied roles at the top of food-webs at Shark Bay and on the GBR, but not at Ningaloo Reef or off the coast of NSW. Composition of δ13C in tissues was influenced by body size and sex of sharks, in addition to residency and diet stability. This variability in stable isotopic composition of tissues is likely to be a result of adaptive foraging strategies that allow these sharks to exploit multiple shelf and offshore habitats. The trophic role of tiger sharks is therefore both context- and habitat-dependent, consistent with a generalist, opportunistic diet at the population level.

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.

Diet and condition of mesopredators on coral reefs in relation to shark abundance.

Reef sharks may influence the foraging behaviour of mesopredatory teleosts on coral reefs via both risk effects and competitive exclusion. We used a "natural experiment" to test the hypothesis that the loss of sharks on coral reefs can influence the diet and body condition of mesopredatory fishes by comparing two remote, atoll-like reef systems, the Rowley Shoals and the Scott Reefs, in northwestern Australia. The Rowley Shoals are a marine reserve where sharks are abundant, whereas at the Scott Reefs numbers of sharks have been reduced by centuries of targeted fishing. On reefs where sharks were rare, the gut contents of five species of mesopredatory teleosts largely contained fish while on reefs with abundant sharks, the same mesopredatory species consumed a larger proportion of benthic invertebrates. These measures of diet were correlated with changes in body condition, such that the condition of mesopredatory teleosts was significantly poorer on reefs with higher shark abundance. Condition was defined as body weight, height and width for a given length and also estimated via several indices of condition. Due to the nature of natural experiments, alternative explanations cannot be discounted. However, the results were consistent with the hypothesis that loss of sharks may influence the diet and condition of mesopredators and by association, their fecundity and trophic role. Regardless of the mechanism (risk effects, competitive release, or other), our findings suggest that overfishing of sharks has the potential to trigger trophic cascades on coral reefs and that further declines in shark populations globally should be prevented to protect ecosystem health.

Predicting occurrence of juvenile shark habitat to improve conservation planning.

Fishing and habitat degradation have increased the extinction risk of sharks, and conservation strategies recognize that survival of juveniles is critical for the effective management of shark populations. Despite the rapid expansion of marine protected areas (MPAs) globally, the paucity of shark-monitoring data on large scales (100s-1000s km) means that the effectiveness of MPAs in halting shark declines remains unclear. Using data collected by baited remote underwater video systems (BRUVS) in northwestern Australia, we developed generalized linear models to elucidate the ecological drivers of habitat suitability for juvenile sharks. We assessed occurrence patterns at the order and species levels. We included all juvenile sharks sampled and the 3 most abundant species sampled separately (grey reef [Carcharhinus amblyrhynchos], sandbar [Carcharhinus plumbeus], and whitetip reef sharks [Triaenodon obesus]). We predicted the occurrence of juvenile sharks across 490,515 km2 of coastal waters and quantified the representation of highly suitable habitats within MPAs. Our species-level models had higher accuracy (ĸ ≥ 0.69) and deviance explained (≥48%) than our order-level model (ĸ = 0.36 and deviance explained of 10%). Maps of predicted occurrence revealed different species-specific patterns of highly suitable habitat. These differences likely reflect different physiological or resource requirements between individual species and validate concerns over the utility of conservation targets based on aggregate species groups as opposed to a species-focused approach. Highly suitable habitats were poorly represented in MPAs with the most restrictions on extractive activities. This spatial mismatch possibly indicates a lack of explicit conservation targets and information on species distribution during the planning process. Non-extractive BRUVS provided a useful platform for building the suitability models across large scales to assist conservation planning across multiple maritime jurisdictions, and our approach provides a simple for method for testing the effectiveness of MPAs.

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.

The ecological connectivity of whale shark aggregations in the Indian Ocean: a photo-identification approach.

Genetic and modelling studies suggest that seasonal aggregations of whale sharks (Rhincodon typus) at coastal sites in the tropics may be linked by migration. Here, we used photo-identification (photo-ID) data collected by both citizen scientists and researchers to assess the connectedness of five whale shark aggregation sites across the entire Indian Ocean at timescales of up to a decade. We used the semi-automated program I3S (Individual Interactive Identification System) to compare photographs of the unique natural marking patterns of individual whale sharks collected from aggregations at Mozambique, the Seychelles, the Maldives, Christmas Island (Australia) and Ningaloo Reef (Australia). From a total of 6519 photos, we found no evidence of connectivity of whale shark aggregations at ocean-basin scales within the time frame of the study and evidence for only limited connectivity at regional (hundreds to thousands of kilometres) scales. A male whale shark photographed in January 2010 at Mozambique was resighted eight months later in the Seychelles and was the only one of 1724 individuals in the database to be photographed at more than one site. On average, 35% of individuals were resighted at the same site in more than one year. A Monte Carlo simulation study showed that the power of this photo-ID approach to document patterns of emigration and immigration was strongly dependent on both the number of individuals identified in aggregations and the size of resident populations.