Abiotic drivers of the space use and activity of gray reef sharks Carcharhinus amblyrhynchos in a dynamic tidal environment.

Predators display rhythms in behavior and habitat use, often with the goal of maximizing foraging success. The underlying mechanisms behind these rhythms are generally linked to abiotic conditions related to diel, lunar, or seasonal cycles. To understand their effects on the space use, activity, and swimming depth of gray reef sharks (Carcharhinus amblyrhynchos), we tagged 38 individuals with depth and accelerometer sensors in a French Polynesian atoll channel exposed to strong tidal flow, and monitored them over a year. C. amblyrhynchos used a larger space during nighttime and were more active at night and during outgoing currents. Shark activity also peaked during the full and new moons. The swimming depth of sharks was mostly influenced by diel cycles, with sharks swimming deeper during the day compared to nighttime. The dynamic energyscape may promote the emergence of discrete behavioral strategies in reef sharks that use the south channel of Fakarava for resting and foraging purposes. Turbulence imposed by outgoing tides induces additional foraging cost on sharks, shifting their hunting areas to the southern part of the channel, where turbulence is less pronounced. Understanding when and where sharks are active and foraging is important for our understanding of predator-prey dynamics and ecosystem dynamics. This study highlights how abiotic rhythms in a highly dynamic environment likely generate spatiotemporal heterogeneity in the distribution of predation pressure.

Behavioural heterogeneity across killer whale social units in their response to feeding opportunities from fisheries.

Intra-population heterogeneity in the behavioural response of predators to changes in prey availability caused by human activities can have major evolutionary implications. Among these activities, fisheries, while extracting resources, also provide new feeding opportunities for marine top predators. However, heterogeneity in the extent to which individuals have responded to these opportunities within populations is poorly understood. Here, we used 18 years of photo-identification data paired with statistical models to assess variation in the way killer whale social units within a subantarctic population (Crozet Islands) interact with fisheries to feed on fish caught on fishing gear (i.e., depredation behaviour). Our results indicate large heterogeneity in both the spatial and temporal extents of depredation across social units. While some frequently depredated on fishery catches over large areas, others sporadically did so and in small areas consistently over the years. These findings suggest that killer whale social units are exposed to varying levels of impacts of depredation, both negative (potential retaliation from fishers) and positive (food provisioning), on their life history traits, and may explain the contrasted demographic patterns observed within the declining population at Crozet but also potentially within the many other killer whale populations documented depredating on fisheries catches worldwide.

Provisioning ecotourism does not increase tiger shark site fidelity.

A perennial criticism of provisioning ecotourism is that it alters the natural behavior and ecology of the target species by providing an artificial food source. Here we evaluate its impact on the long-term site fidelity patterns of tiger sharks in French Polynesia. We hypothesized that a significant impact of provisioning would lead to (1) increases in individual site fidelity over time, and (2) an increase in the number of resident individuals over time. Of 53 individuals photo-identified and monitored during > 500 dives over five years, 10 individuals accounted for > 75% of all sightings, whereas 35 sharks were sighted very infrequently. Even the most frequently observed tiger sharks exhibited overall low fidelity at the site and showed no increase in site fidelity over time. Furthermore, the number of tiger sharks sighted during each dive did not increase. The observed patterns of tiger shark sightings were best explained by natural movements, including general roaming within home ranges along the coastline and seasonal migrations. Despite the apparent lack of impact of provisioning ecotourism on tiger shark ecology in Tahitian waters, it would be prudent to implement a strict code of conduct during any future provisioning activities to maximize the safety of participants and animals involved.

Citizen science provides valuable data to evaluate elasmobranch diversity and trends throughout the French Polynesia's shark sanctuary.

Observers of the Polynesian Shark Observatory (ORP), a citizen science network organized mainly through the Polynesian dive centers, collected an unprecedented amount of data from more than 13,916 dives spanning 43% of the islands of French Polynesia between July 8, 2011, and April 11, 2018. The objective for this type of data collection, which is not accessible within the standard research context, was to provide a unique dataset, and the opportunity to explore the specific diversity, distribution, seasonality and abundance of many elasmobranch species spread out throughout the territory of French Polynesia. Since the data are based on random citizen observations, the spatial distribution was biased toward the most frequented sites and islands where scuba diving is most developed. Overall, the increase in observed abundance of rays and sharks observed in French Polynesia, and the three most sampled islands as well as the high specific diversity recorded for the region, provide first evidence on the effectiveness of the French Polynesia's Shark Sanctuary, established in 2006. These data, collected randomly by the volunteers, also provide insights into potential movement patterns and site fidelity of some of the more commonly observed species. While no final conclusions can be drawn, it is clear that the network of volunteers that regularly contributes information to the Polynesian Shark Observatory plays a very important role in the delivery of much needed data for conservation and management action, as well as providing perspectives for new directions in research on sharks and rays in French Polynesia.

Like a rolling stone: Colonization and migration dynamics of the gray reef shark (Carcharhinus amblyrhynchos).

Designing appropriate management plans requires knowledge of both the dispersal ability and what has shaped the current distribution of the species under consideration. Here, we investigated the evolutionary history of the endangered gray reef shark (Carcharhinus amblyrhynchos) across its range by sequencing thousands of RADseq loci in 173 individuals in the Indo-Pacific (IP). We first bring evidence of the occurrence of a range expansion (RE) originating close to the Indo-Australian Archipelago (IAA) where two stepping-stone waves (east and westward) colonized almost the entire IP. Coalescent modeling additionally highlighted a homogenous connectivity (Nm ~ 10 per generation) throughout the range, and isolation by distance model suggested the absence of barriers to dispersal despite the affinity of C. amblyrhynchos to coral reefs. This coincides with long-distance swims previously recorded, suggesting that the strong genetic structure at the IP scale (F ST ~ 0.56 between its ends) is the consequence of its broad current distribution and organization in a large number of demes. Our results strongly suggest that management plans for the gray reef shark should be designed on a range-wide rather than a local scale due to its continuous genetic structure. We further contrasted these results with those obtained previously for the sympatric but strictly lagoon-associated Carcharhinus melanopterus, known for its restricted dispersal ability. Carcharhinus melanopterus exhibits a similar RE dynamic but is characterized by a stronger genetic structure and a nonhomogeneous connectivity largely dependent on local coral reefs availability. This sheds new light on shark evolution, emphasizing the roles of IAA as source of biodiversity and of life-history traits in shaping the extent of genetic structure and diversity.

A Wireless Autonomous Real-Time Underwater Acoustic Positioning System.

Recent acoustic telemetry positioning systems are able to reconstruct the positions and trajectories of organisms at a scale of a few centimeters to a few meters. However, they present several logistical constraints including receiver maintenance, calibration procedures and limited access to real-time data. We present here a novel, easy-to-deploy, energy self-sufficient underwater positioning system based on the time difference of arrival (TDOA) algorithm and the Global System for Mobile (GSM) communication technology, capable of locating tagged marine organisms in real time. We provide an illustration of the application of this system with empirical examples using continuous and coded tags in fish and benthic invertebrates. In situ experimental tests of the operational system demonstrated similar performances to currently available acoustic positioning systems, with a global positioning error of 7.13 ± 5.80 m (mean ± SD) and one-third of the pings can be localized within 278 m of the farthest buoy. Despite some required improvements, this prototype is designed to be autonomous and can be deployed from the surface in various environments (rivers, lakes, and oceans). It was proven to be useful to monitor a wide variety of species (benthic and pelagic) in real time. Its real-time property can be used to rapidly detect system failure, optimize deployment design, or for ecological or conservation applications.

Let them go free: Spatial behaviour following the experimental release of hatchery-reared juveniles Sciaena umbra and Dentex dentex.

As marine stocks and biodiversity are rapidly declining, the release of hatchery-reared individuals into the wild is a species conservation measure aiming at replenishing stocks of freshwater, anadromous and marine fish species. The aim of this study is to assess for the first time the post-release exploration behaviours, survival and dispersal in the wild of released hatchery-reared juveniles of D. dentex and S. umbra. For this purpose, twenty fish from each species were tagged with acoustic transmitters and released in a marine no-take zone located in Corsica (France). Most individuals were considered alive until their last detection (95% of S. umbra and 74% of D. dentex detected individuals). Fish were detected within the receiver array on average up to 11.3 (± 20.7) and 10.3 (± 10.3) days after being released for juveniles of D. dentex and S.umbra, respectively. Dentex dentex juveniles dispersed mostly southward along the shore whereas S. umbra juveniles tended to disperse along the shore both northward and southward from the acoustic receiver array. Before their rapid dispersion (i.e. within a few days) outside the studied zone, juveniles of both species displayed increasing cumulative MCP areas and increased their vertical niche revealing their gradual coverage and exploration of deeper habitats in the area. The results from our study highlighted that hatchery-reared juveniles of both species did not settle inside the studied area but seemed to start to acclimate to the natural environment. This work is a first step towards the assessment of the viability of restocking for both species.

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.

Social dynamics and individual hunting tactics of white sharks revealed by biologging.

Social foraging, where animals forage in groups, takes many forms but is less studied in marine predators as measuring social associations in the wild is challenging. We used biologging (activity, cameras and telemetry receivers) sensors to measure social associations and simultaneous behaviour, in white sharks (Carcharodon carcharias) off Guadalupe Island, Mexico. Animal-borne telemetry receivers revealed that sharks varied in the number of associations they formed and occurred most often when sharks were swimming in straight paths or when they were turning frequently. While many associations were likely random, there was evidence of some stronger associations. Sharks varied in the depths they used and their activity, with some individuals more active in shallow water while others were more active 200-300 m deep. We propose that white sharks associate with other individuals so they can inadvertently share information on the location or remains of large prey. However, there may be a wide range of individual variability in both behaviour and sociality. Biologging now enables social associations of animals to be measured, concurrent with measures of their behaviour, so that social foraging of large marine predators can be quantified in the wild.

Social networks and the conservation of fish.

Despite our critical dependence on aquatic wildlife, we lack a complete understanding of the drivers of population stability and structure for most fish species. Social network analysis has been increasingly used to investigate animal societies as it explicitly links individual decision-making to population-level processes and demography. While the study of social structure is of great ecological interest, it is also potentially important for species of economic value or of conservation concern. To date however, there has been little focus on how social processes are likely to influence the conservation of fish populations. Here we identify applications for how a social network approach can help address broad fish conservation themes such as population structure, biological invasions or fisheries management. We discuss the burgeoning opportunities offered and challenges still faced by current technologies to integrate social network approaches within fish conservation.

Effects of a COVID-19 lockdown-induced pause and resumption of artificial provisioning on blacktip reef sharks (Carcharhinus melanopterus) and pink whiprays (Pateobatis fai) in French Polynesia (East-Pacific).

The tourism activities linked to artificial provisioning of blacktip reef sharks (Carcharhinus melanopterus) and pink whiprays (Pateobatis fai) on a specific site in French Polynesia were suddenly and completely stopped due to a COVID-19 lockdown that lasted 6 weeks from March 20 until April 30, 2020. Using both drone footage and underwater counting, we were able to track the abundance of those two species before, during, and after reopening and thus investigate the impact of provisioning on wild shark populations. The absence of any stimulus during this long period resulted in almost total desertion of the site by the elasmobranchs. However, 1 day prior to reopening, some individuals of both species positively reacted to the single acoustic stimulus of an engine boat, showing the resilience of conditioning, and some elasmobranchs reacted to acoustic and olfactive stimuli linked to the provisioning practice from the first day after reopening. During the first 2 weeks after reopening, the abundance of both species remained at reduced levels comparable to those observed between 2008 and 2010 for sharks; i.e., around 9 animals in the presence of local tourists. Pre-lockdown abundance levels, reaching approximatively 15 individuals for sharks and 10 for rays, were considered restored 1 and 2 months after reopening for blacktip reef sharks and pink whiprays, respectively. These findings improve our capacity to better understand the potential effects of artificial provisioning tourism on the abundance of elasmobranchs by showing that conditioning is resilient for several weeks, suggesting that intermittent interruption of elasmobranchs feeding would not really help to decrease its impact on animal welfare.

Residency and movement patterns of adult Port Jackson sharks (Heterodontus portusjacksoni) at a breeding aggregation site.

Examining the movement ecology of mesopredators is fundamental to developing an understanding of their biology, ecology and behaviour, as well as the communities and ecosystems they influence. The limited research on the residency and movements of benthic marine mesopredators has primarily used visual tags, which do not allow for the efficient and accurate monitoring of individual space use. In this study, the authors investigated the residency and movement patterns of Port Jackson sharks Heterodontus portusjacksoni (Meyer 1793) at a breeding aggregation site in Jervis Bay, south-eastern Australia, using passive acoustic telemetry to further our understanding of the movement ecology of these important mesopredators. Between 2012 and 2014, individuals were tagged with acoustic transmitters, and their residency and movements within the bay were monitored for up to 4 years. H. portusjacksoni showed strong preferences for particular reefs within and between breeding seasons. Males had significantly higher residency indices at their favoured sites relative to females, suggesting that males may be engaging in territorial behaviour. Conversely, female H. portusjacksoni exhibited higher roaming indices relative to males indicating that females may move between sites to assess males. Finally, H. portusjacksoni showed temporal variation in movements between reefs with individuals typically visiting more reefs at night relative to the day, dusk and dawn corresponding with their nocturnal habits.

Sharks surf the slope: Current updrafts reduce energy expenditure for aggregating marine predators.

An animal's energy landscape considers the power requirements associated with residing in or moving through habitats. Within marine environments, these landscapes can be dynamic as water currents will influence animal power requirements and can change rapidly over diel and tidal cycles. In channels and along slopes with strong currents, updraft zones may reduce energy expenditure of negatively buoyant fishes that are also obligate swimmers. Despite marine predators often residing within high-current area, no study has investigated the potential role of the energetic landscape in driving such habitat selectivity. Over 500 grey reef sharks Carcharhinus amblyrhynchos reside in the southern channel of Fakarava Atoll, French Polynesia. We used diver observations, acoustic telemetry and biologging to show that sharks use regions of predicted updrafts and switch their core area of space use based on tidal state (incoming versus outgoing). During incoming tides, sharks form tight groups and display shuttling behaviour (moving to the front of the group and letting the current move them to the back) to maintain themselves in these potential updraft zones. During outgoing tides, group dispersion increases, swimming depths decrease and shuttling behaviours cease. These changes are likely due to shifts in the nature and location of the updraft zones, as well as turbulence during outgoing tides. Using a biomechanical model, we estimate that routine metabolic rates for sharks may be reduced by 10%-15% when in updraft zones. Grey reef sharks save energy using predicted updraft zones in channels and 'surfing the slope'. Analogous to birds using wind-driven updraft zones, negatively buoyant marine animals may use current-induced updraft zones to reduce energy expenditure. Updrafts should be incorporated into dynamic energy landscapes and may partially explain the distribution, behaviour and potentially abundance of marine predators.

Investigating links between thermal tolerance and oxygen supply capacity in shark neonates from a hyperoxic tropical environment.

Temperature and oxygen limit the distribution of marine ectotherms. Haematological traits underlying blood-oxygen carrying capacity are thought to be correlated with thermal tolerance in certain fishes, and this relationship is hypothesised to be explained by oxygen supply capacity. We tested this hypothesis using reef shark neonates as experimental models because they live near their upper thermal limits and are physiologically sensitive to low oxygen conditions. We first described in situ associations between temperature and oxygen at the study site (Moorea, French Polynesia) and found that the habitats for reef shark neonates (Carcharhinus melanopterus and Negaprion acutidens) were hyperoxic at the maximum recorded temperatures. Next, we tested for in situ associations between thermal habitat characteristics and haematological traits of neonates. Contrary to predictions, we only demonstrated a negative association between haemoglobin concentration and maximum habitat temperatures in C. melanopterus. Next, we tested for ex situ associations between critical thermal maximum (CTMax) and haematological traits, but only demonstrated a negative association between haematocrit and CTMax in C. melanopterus. Finally, we measured critical oxygen tension (pcrit) ex situ and estimated its temperature sensitivity to predict oxygen-dependent values of CTMax. Estimated temperature sensitivity of pcrit was similar to reported values for sharks and skates, and predicted values for CTMax equalled maximum habitat temperatures. These data demonstrate unique associations between haematological traits and thermal tolerance in a reef shark that are likely not explained by oxygen supply capacity. However, a relationship between oxygen supply capacity and thermal tolerance remains to be demonstrated empirically.

Response of blacktip reef sharks Carcharhinus melanopterus to shark bite mitigation products.

Globally, the frequency of shark bites is rising, resulting in an increasing demand for shark deterrents and measures to lessen the impact of shark bites on humans. Most existing shark protection measures are designed to reduce the probability of a bite, but fabrics that minimise injuries when a shark bite occurs can also be used as mitigation devices. Here, we assessed the ability of the Ocean Guardian Scuba7 and Kevlar material to reduce the likelihood of blacktip reef sharks, Carcharhinus melanopterus, from feeding, and to minimise injuries from shark bites. Sharks were enticed to consume a small piece of local reef fish (bait) placed between the two Scuba7 electrodes with the deterrents randomly being turned on or kept off. In the second experiment, the bait was attached to a small pouch made of either standard neoprene or neoprene with a protective layer of Kevlar around it. The Scuba7 reduced the proportion of baits being taken by 67%, (from 100% during control trials to 33%). Sharks also took more time to take the bait when the device was active (165 ± 20.40 s vs. 38.9 ± 3.35 s), approached at a greater distance (80.98 ± 1.72 cm vs. 38.88 ± 3.20 cm) and made a greater number of approaches per trial (19.38 ± 2.29 vs. 3.62 ± 0.53) than when the Scuba7 was inactive. The sizes of punctures from shark bites were significantly smaller on neoprene with Kevlar compared to standard neoprene (3.64 ± 0.26 mm vs. 5.88 ± 0.29 mm). The number of punctures was also fewer when Kevlar was used (14.92 ± 3.16 vs. 74.1 ± 12.44). Overall, the Ocean Guardian Scuba7 and Kevlar reduced the impact of blacktip reef shark bites. These findings may help consumers make informed decisions when purchasing shark deterring and protective products.

Acoustic accelerometry reveals diel activity patterns in premigratory Port Jackson sharks.

Distinguishing the factors that influence activity within a species advances understanding of their behavior and ecology. Continuous observation in the marine environment is not feasible but biotelemetry devices provide an opportunity for detailed analysis of movements and activity patterns. This study investigated the detail that calibration of accelerometers measuring root mean square (RMS) acceleration with video footage can add to understanding the activity patterns of male and female Port Jackson sharks (Heterodontus portusjacksoni) in a captive environment. Linear regression was used to relate RMS acceleration output to time-matched behavior captured on video to quantify diel activity patterns. To validate captive data, diel patterns from captive sharks were compared with diel movement data from free-ranging sharks using passive acoustic tracking. The RMS acceleration data showed captive sharks exhibited nocturnal diel patterns peaking during the late evening before midnight and decreasing before sunrise. Correlation analysis revealed that captive animals displayed similar activity patterns to free-ranging sharks. The timing of wild shark departures for migration in the late breeding season corresponded with elevated diel activity at night within the captive individuals, suggesting a form of migratory restlessness in captivity. By directly relating RMS acceleration output to activity level, we show that sex, time of day, and sex-specific seasonal behavior all influenced activity levels. This study contributes to a growing body of evidence that RMS acceleration data are a promising method to determine activity patterns of cryptic marine animals and can provide more detailed information when validated in captivity.

A DNA barcode reference library of French Polynesian shore fishes.

The emergence of DNA barcoding and metabarcoding opened new ways to study biological diversity, however, the completion of DNA barcode libraries is fundamental for such approaches to succeed. This dataset is a DNA barcode reference library (fragment of Cytochrome Oxydase I gene) for 2,190 specimens representing at least 540 species of shore fishes collected over 10 years at 154 sites across the four volcanic archipelagos of French Polynesia; the Austral, Gambier, Marquesas and Society Islands, a 5,000,000 km2 area. At present, 65% of the known shore fish species of these archipelagoes possess a DNA barcode associated with preserved, photographed, tissue sampled and cataloged specimens, and extensive collection locality data. This dataset represents one of the most comprehensive DNA barcoding efforts for a vertebrate fauna to date. Considering the challenges associated with the conservation of coral reef fishes and the difficulties of accurately identifying species using morphological characters, this publicly available library is expected to be helpful for both authorities and academics in various fields.

Inter-individual differences in ontogenetic trophic shifts among three marine predators.

Ontogenetic niche shifts are widespread. However, individual differences in size at birth, morphology, sex, and personalities can cause variability in behavior. As such, inherent inter-individual differences within populations may lead to context-dependent changes in behavior with animal body size, which is of concern for understanding population dynamics and optimizing ecological monitoring. Using stable carbon and nitrogen isotope values from concurrently sampled tissues, we quantified the direction and magnitude of intraspecific variation in trophic shifts among three shark species, and how these changed with body size: spurdogs (Squalus spp.) in deep-sea habitats off La Réunion, bull sharks (Carcharhinus leucas) in estuarine habitats of the Florida Everglades, and blacktip reef sharks (Carcharhinus melanopterus) in coral reef ecosystems of Moorea, French Polynesia. Intraspecific variation in trophic shifts was limited among spurdogs, and decreased with body size, while bull sharks exhibited greater individual differences in trophic shifts, but also decreased in variability through ontogeny. In contrast, blacktip reef sharks exhibited increased intraspecific variation in trophic interactions with body size. Variability in trophic interactions and ontogenetic shifts are known to be associated with changes in energetic requirements, but can vary with ecological context. Our results suggest that environmental stability may affect variability within populations, and ecosystems with greater spatial and/or temporal variability in environmental conditions, and those with more diverse food webs may facilitate greater individual differences in trophic interactions, and thus ontogenetic trophic shifts. In light of concerns over environmental disturbance, elucidating the contexts that promote or dampen phenotypic variability is invaluable for predicting population- and community-level responses to environmental changes.

Using unmanned aerial vehicle (UAV) surveys and image analysis in the study of large surface-associated marine species: a case study on reef sharks Carcharhinus melanopterus shoaling behaviour.

A novel image analysis-based technique applied to unmanned aerial vehicle (UAV) survey data is described to detect and locate individual free-ranging sharks within aggregations. The method allows rapid collection of data and quantification of fine-scale swimming and collective patterns of sharks. We demonstrate the usefulness of this technique in a small-scale case study exploring the shoaling tendencies of blacktip reef sharks Carcharhinus melanopterus in a large lagoon within Moorea, French Polynesia. Using our approach, we found that C. melanopterus displayed increased alignment with shoal companions when distributed over a sandflat where they are regularly fed for ecotourism purposes as compared with when they shoaled in a deeper adjacent channel. Our case study highlights the potential of a relatively low-cost method that combines UAV survey data and image analysis to detect differences in shoaling patterns of free-ranging sharks in shallow habitats. This approach offers an alternative to current techniques commonly used in controlled settings that require time-consuming post-processing effort.