Barau's petrel, Pterodroma baraui, as a bioindicator of plastic pollution in the South-West Indian Ocean: A multifaceted approach.

Marine plastic pollution is well described by bioindicator species in temperate and polar regions but remains understudied in tropical oceans. We addressed this gap by evaluating the seabird Barau's petrel as bioindicator of plastic pollution in the South-West Indian Ocean. We conducted a multifaceted approach including necropsies of birds to quantify plastic ingestion; GPS tracking of breeding adults to identify their foraging areas; manta trawling of plastic debris to measure plastic pollution at sea and modelling of plastic dispersal. We developed a spatial risk index of seabird exposure to plastic ingestion. Seventy-one percent of the analysed birds had ingested plastic. GPS tracking coupled with manta trawling and dispersal modelling show that adults consistently foraged at places with high level of plastic concentration. The highest ingestion risk occurred in the northwest of Reunion Island and at latitude 30°S. Our findings confirm that Barau's petrel is a reliable bioindicator of plastic pollution in the region.

Seabird nutrient subsidies enrich mangrove ecosystems and are exported to nearby coastal habitats.

Eutrophication by human-derived nutrient enrichment is a major threat to mangroves, impacting productivity, ecological functions, resilience, and ecosystem services. Natural mangrove nutrient enrichment processes, however, remain largely uninvestigated. Mobile consumers such as seabirds are important vectors of cross-ecosystem nutrient subsidies to islands but how they influence mangrove ecosystems is poorly known. We assessed the contribution, uptake, cycling, and transfer of nutrients from seabird colonies in remote mangrove systems free of human stressors. We found that nutrients from seabird guano enrich mangrove plants, reduce nutrient limitations, enhance mangrove invertebrate food webs, and are exported to nearby coastal habitats through tidal flow. We show that seabird nutrient subsidies in mangroves can be substantial, improving the nutrient status and health of mangroves and adjacent coastal habitats. Conserving mobile consumers, such as seabirds, is therefore vital to preserve and enhance their role in mangrove productivity, resilience, and provision of diverse functions and services.

Ontogenetic shifts in body form in the bull shark Carcharhinus leucas.

Recent studies have uncovered mosaic patterns of allometric and isometric growth underlying ontogenetic shifts in the body form of elasmobranch species (shark and rays). It is thought that shifts in trophic and spatial ecology through ontogeny drive these morphological changes; however, additional hypotheses relating to developmental constraints have also been posed. The bull shark (Carcharhinus leucas) is a large-bodied coastal shark that exhibits strong ontogenetic shifts in trophic and spatial ecology. In this study, we utilise a large data set covering a large number of morphological structures to reveal ontogenetic shifts in the body form of C. leucas, stratifying analyses by sex and size classes to provide fine-scale, more ecomorphologically relevant results. Our results indicate shifts in functional demands across the body through ontogeny, driven by selective pressures relating to trophic and spatial ecology driving the evolution of allometry. We also find significant differences in scaling trends between life stages, and between the sexes, highlighting the importance of utilising large, diverse datasets that can be stratified in this way to improve our understanding of elasmobranch morphological evolution. Ultimately, we discuss the implications of these results for existing ecomorphological hypotheses regarding the evolution of specific morphological structures, and pose novel hypotheses where relevant.

From rivers to ocean basins: The role of ocean barriers and philopatry in the genetic structuring of a cosmopolitan coastal predator.

The Bull Shark (Carcharhinus leucas) faces varying levels of exploitation around the world due to its coastal distribution. Information regarding population connectivity is crucial to evaluate its conservation status and local fishing impacts. In this study, we sampled 922 putative Bull Sharks from 19 locations in the first global assessment of population structure of this cosmopolitan species. Using a recently developed DNA-capture approach (DArTcap), samples were genotyped for 3400 nuclear markers. Additionally, full mitochondrial genomes of 384 Indo-Pacific samples were sequenced. Reproductive isolation was found between and across ocean basins (eastern Pacific, western Atlantic, eastern Atlantic, Indo-West Pacific) with distinct island populations in Japan and Fiji. Bull Sharks appear to maintain gene flow using shallow coastal waters as dispersal corridors, whereas large oceanic distances and historical land-bridges act as barriers. Females tend to return to the same area for reproduction, making them more susceptible to local threats and an important focus for management actions. Given these behaviors, the exploitation of Bull Sharks from insular populations, such as Japan and Fiji, may instigate local decline that cannot readily be replenished by immigration, which can in turn affect ecosystem dynamics and functions. These data also supported the development of a genetic panel to ascertain the population of origin, which will be useful in monitoring the trade of fisheries products and assessing population-level impacts of this harvest.

Isotopic niche partitioning of co-occurring large marine vertebrates around an Indian ocean tropical oceanic island.

Tropical oceans host a high diversity of species, including large marine consumers. In these oligotrophic ecosystems, oceanic islands often favour the aggregation of species and biomass as they provide feeding opportunities related to the mechanisms of island mass effect. As such, the waters surrounding La Reunion (Southwest Indian Ocean) host seabirds, large pelagic teleosts, elasmobranchs, delphinids and sea turtles. Isotopic niche partitioning and comparison of trophic levels among these species (n = 21) were investigated using stable carbon (δ13C) and nitrogen (δ15N) isotope analysis. Overall, δ13C values were highly variable among taxa, indicating that the species exploit multiple foraging habitats along a coast-open ocean gradient. Overlap in δ15N values was limited, except for teleost species, the two species of sea turtles and two species of delphinids, the Indo-pacific bottlenose dolphin (Tursiops aduncus) and the Spinner dolphin (Stellena longirostris). Stable isotope analyses of samples collected over a 9-years period on different tissues with different integration times provide a consistent picture of the structure of the community of large marine vertebrates species around La Reunion and highlight the underlying mechanisms to limit the competition between species. The wide range of isotopic values confirms that large marine vertebrates have different trophic roles in coastal marine food webs around this oceanic island, which limits their potential of competitive interactions for resources.

Ecological and biogeographic features shaped the complex evolutionary history of an iconic apex predator (Galeocerdo cuvier).

BACKGROUND: The tiger shark (Galeocerdo cuvier) is a large iconic marine predator inhabiting worldwide tropical and subtropical waters. So far, only mitochondrial markers and microsatellites studies have investigated its worldwide historical demography with inconclusive outcomes. Here, we assessed for the first time the genomic variability of tiger shark based on RAD-seq data for 50 individuals from five sampling sites in the Indo-Pacific (IP) and one in the Atlantic Ocean (AO) to decipher the extent of the species' global connectivity and its demographic history. RESULTS: Clustering algorithms (PCA and NMF), FST and an approximate Bayesian computation framework revealed the presence of two clusters corresponding to the two oceanic basins. By modelling the two-dimensional site frequency spectrum, we tested alternative isolation/migration scenarios between these two identified populations. We found the highest support for a divergence time between the two ocean basins of ~ 193,000 years before present (B.P) and an ongoing but limited asymmetric migration ~ 176 times larger from the IP to the AO (Nm ~ 3.9) than vice versa (Nm ~ 0.02). CONCLUSIONS: The two oceanic regions are isolated by a strong barrier to dispersal more permeable from the IP to the AO through the Agulhas leakage. We finally emphasized contrasting recent demographic histories for the two regions, with the IP characterized by a recent bottleneck around 2000 years B.P. and the AO by an expansion starting 6000 years B.P. The large differentiation between the two oceanic regions and the absence of population structure within each ocean basin highlight the need for two large management units and call for future conservation programs at the oceanic rather than local scale, particularly in the Indo-Pacific where the population is declining.

Forensic genetic identification of sharks involved in human attacks.

Each year, 75-100 unprovoked shark attacks on humans are recorded, most of them resulting in no or minor injuries, while a few are fatal. Often, shark identification responsible for attacks relies on visual observations or bite wound characteristics, which limits species determination and preclude individual identification. Here, we provide two genetic approaches to reliably identify species and/or individuals involved in shark attacks on humans based on a non-invasive DNA sampling (i.e. DNA traces present on bite wounds on victims), depending on the knowledge of previous attack history at the site. The first approach uses barcoding techniques allowing species identification without any a priori, while the second relies on microsatellite genotyping, allowing species identification confirmation and individual identification, but requiring an a priori of the potential species involved in the attack. Both approaches were validated by investigating two shark attacks that occurred in Reunion Island (southwestern Indian Ocean). According to both methods, each incident was attributed to a bull shark (Carcharhinus leucas), in agreement with suggestions derived from bite wound characteristics. Both approaches appear thus suitable for the reliable identification of species involved in shark attacks on humans. Moreover, microsatellite genotyping reveals, in the studied cases, that two distinct individuals were responsible of the bites. Applying these genetic identification methods will resolve ambiguities on shark species involved in attacks and allow the collection of individual data to better understand and mitigate shark risk.

Age and growth of the bull shark (Carcharhinus leucas) around Reunion Island, South West Indian Ocean.

Sharks exhibit varied demographic strategies depending on both the species and the population location, which make them more or less vulnerable to fishing. Accurate evaluation of local age and growth parameters is therefore fundamental for the sustainable management of their stocks. Although demographic parameters have been assessed for bull shark (Carcharhinus leucas) populations in several locations of the world, this information is missing so far around Reunion Island, in the south-west Indian Ocean. To fill this gap of knowledge, age and growth data were gathered from the vertebrae of 140 individuals of C. leucas (77 females and 63 males, mostly adults) fished around the island between 2012 and 2019. After verification of the annual deposition of growth band pairs on these structures using relative marginal increment analysis on 40 individuals, band pairs were counted along the vertebral centrum for each individual. Thanks to this approach, growth was shown to significantly differ between male and female C. leucas around Reunion Island, with respective von Bertalanffy growth model equations of Lt  =  314 1 - e - 0.0814 t + 5.45 and Lt  = 321.5 1 - e - 0.0999 t + 3.420 . Indeed, the females of the species fished in this area were significantly (P < 0.001) larger than local males, with an estimated difference in size of ~16.1 cm at 20 years old. They also apparently reach older ages, with an estimated maximum age of 33.50 years, against 29.75 years only for the males. The estimated size at birth around the island is larger than elsewhere in the world, varying from 92.30 to 100.00 cm depending on the method used. These results confirm that the population of C. leucas around Reunion Island exhibits a K-selected strategy, which makes it highly vulnerable to fishing pressure.

Mercury isotopes as tracers of ecology and metabolism in two sympatric shark species.

In coastal ecosystems, top predators are exposed to a wide variety of nutrient and contaminant sources due to the diversity of trophic webs within inshore marine habitats. Mercury contamination could represent an additional threat to shark populations that are declining worldwide. Here we measured total mercury, carbon and nitrogen isotopes, as well as mercury isotopes, in two co-occurring shark species (the bull shark Carcharhinus leucas and the tiger shark Galeocerdo cuvier) and their potential prey from a coastal ecosystem of the western Indian Ocean (La Réunion Island). Our primary goals were to (i) determine the main trophic Hg sources for sharks and (ii) better characterize their diet composition and foraging habitat. Hg isotope signatures (Δ199Hg and δ202Hg) of shark prey suggested that bull sharks were exposed to methylmercury (MeHg) produced in offshore epipelagic waters, while tiger sharks were exposed to offshore mesopelagic MeHg with additional microbial transformation in slope sediments. Δ199Hg values efficiently traced the ecology of the two predators, demonstrating that bull sharks targeted coastal prey in shallow waters while tiger sharks were mainly foraging on mesopelagic species in the deeper waters of the island slope. Unexpectedly, we found a positive shift in δ202Hg (>1‰) between sharks and their prey, leading to high δ202Hg values in the two shark species (e.g. 1.91 ± 0.52‰ in bull sharks). This large shift in δ202Hg indicates that sharks may display strong MeHg demethylation abilities, possibly reflecting evolutionary pathways for mitigating their MeHg contamination.

Population structure, connectivity, and demographic history of an apex marine predator, the bull shark Carcharhinus leucas.

Knowledge of population structure, connectivity, and effective population size remains limited for many marine apex predators, including the bull shark Carcharhinus leucas. This large-bodied coastal shark is distributed worldwide in warm temperate and tropical waters, and uses estuaries and rivers as nurseries. As an apex predator, the bull shark likely plays a vital ecological role within marine food webs, but is at risk due to inshore habitat degradation and various fishing pressures. We investigated the bull shark's global population structure and demographic history by analyzing the genetic diversity of 370 individuals from 11 different locations using 25 microsatellite loci and three mitochondrial genes (CR, nd4, and cytb). Both types of markers revealed clustering between sharks from the Western Atlantic and those from the Western Pacific and the Western Indian Ocean, with no contemporary gene flow. Microsatellite data suggested low differentiation between the Western Indian Ocean and the Western Pacific, but substantial differentiation was found using mitochondrial DNA. Integrating information from both types of markers and using Bayesian computation with a random forest procedure (ABC-RF), this discordance was found to be due to a complete lack of contemporary gene flow. High genetic connectivity was found both within the Western Indian Ocean and within the Western Pacific. In conclusion, these results suggest important structuring of bull shark populations globally with important gene flow occurring along coastlines, highlighting the need for management and conservation plans on regional scales rather than oceanic basin scale.

Reproductive biology, multiple paternity and polyandry of the bull shark Carcharhinus leucas.

To improve understanding of bull shark Carcharhinus leucas reproductive biology, we analysed reproductive traits from 118 bull sharks caught along Reunion Island coasts (Western Indian Ocean), including 16 gravid females. Specific microsatellite loci were used to investigate the frequency of multiple paternity. Males and females reached maturity at c. 234 cm and 257 cm total length (LT ), respectively, and litter sizes ranged from 5 to 14 embryos. Analysis of the 16 litters collected in various months of the year indicated that parturition occurs between October and December, with a size at birth c. 60-80 cm LT and that the gestation period is probably c. 12 months. Assuming a 1 year resting period and a period of sperm storage (4-5 months) between mating (in June-September) and fertilisation, the reproductive cycle of bull sharks at Reunion Island would be biennial. At least 56.25% of the litters investigated were polyandrous, sired by 2-5 males. Several males that each sired several litters conceived during the same or distinct mating seasons were detected, suggesting both a seasonal aggregation of sharks to mate and some male fidelity to mating site. Altogether, these findings provide valuable information for both shark risk management and conservation of the species in the Western Indian Ocean.

Genetic population structure and demography of an apex predator, the tiger shark Galeocerdo cuvier.

Population genetics has been increasingly applied to study large sharks over the last decade. Whilst large shark species are often difficult to study with direct methods, improved knowledge is needed for both population management and conservation, especially for species vulnerable to anthropogenic and climatic impacts. The tiger shark, Galeocerdo cuvier, is an apex predator known to play important direct and indirect roles in tropical and subtropical marine ecosystems. While the global and Indo-West Pacific population genetic structure of this species has recently been investigated, questions remain over population structure and demographic history within the western Indian (WIO) and within the western Pacific Oceans (WPO). To address the knowledge gap in tiger shark regional population structures, the genetic diversity of 286 individuals sampled in seven localities was investigated using 27 microsatellite loci and three mitochondrial genes (CR,COI, and cytb). A weak genetic differentiation was observed between the WIO and the WPO, suggesting high genetic connectivity. This result agrees with previous studies and highlights the importance of the pelagic behavior of this species to ensure gene flow. Using approximate Bayesian computation to couple information from both nuclear and mitochondrial markers, evidence of a recent bottleneck in the Holocene (2,000-3,000 years ago) was found, which is the most probable cause for the low genetic diversity observed. A contemporary effective population size as low as 111 [43,369] was estimated during the bottleneck. Together, these results indicate low genetic diversity that may reflect a vulnerable population sensitive to regional pressures. Conservation measures are thus needed to protect a species that is classified as Near Threatened.

Effect of body length, trophic position and habitat use on mercury concentrations of sharks from contrasted ecosystems in the southwestern Indian Ocean.

The non-essential metal mercury (Hg) can have deleterious effects on health of organisms, and tends to bioaccumulate with age in long-lived organisms and to biomagnify along food webs. Because elasmobranchs are fished for human consumption and their Hg levels are frequently above the maximum Hg concentration recommended for fish consumption, understanding the drivers of Hg concentration is of considerable interest. Total Hg concentrations were analysed in muscle tissues of 14 shark and 2 batoid species (n = 339 individuals) sampled across multiple habitats (coastal, open ocean and bathyal) in the southwestern Indian Ocean. Stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) were analysed to assess whether relative trophic position and foraging habitats affected Hg concentrations. Hg concentrations increased with δ15N and body length, highlighting the mechanisms of bioaccumulation and biomagnification in relation with the trophic position and size of the individuals. Habitats where elasmobranchs were collected also affected their Hg concentrations. Bathyal sharks had high Hg concentrations that were almost similar to those of oceanic species, despite their lower relative trophic position. Higher bioavailability of Hg due to its enhanced methylation in deeper waters was considered as the most likely explanation for this result. These results highlight that multiple factors contribute to mercury accumulation in elasmobranchs.

Accumulate or eliminate? Seasonal mercury dynamics in albatrosses, the most contaminated family of birds.

Albatrosses (Diomedeidae) are iconic pelagic seabirds whose life-history traits (longevity, high trophic position) put them at risk of high levels of exposure to methylmercury (MeHg), a powerful neurotoxin that threatens humans and wildlife. Here, we report total Hg (THg) concentrations in body feathers from 516 individual albatrosses from 35 populations, including all 20 taxa breeding in the Southern Ocean. Our key finding is that albatrosses constitute the family of birds with the highest levels of contamination by Hg, with mean feather THg concentrations in different populations ranging from moderate (3.8 µg/g) to exceptionally high (34.6 µg/g). Phylogeny had a significant effect on feather THg concentrations, with the mean decreasing in the order Diomedea > Phoebetria > Thalassarche. Unexpectedly, moulting habitats (reflected in feather δ13C values) was the main driver of feather THg concentrations, indicating increasing MeHg exposure with decreasing latitude, from Antarctic to subtropical waters. The role of moulting habitat suggests that the majority of MeHg eliminated into feathers by albatrosses is from recent food intake (income strategy). They thus differ from species that depurate MeHg into feathers that has been accumulated in internal tissues between two successive moults (capital strategy). Since albatrosses are amongst the most threatened families of birds, it is noteworthy that two albatrosses listed as Critical by the World Conservation Union (IUCN) that moult and breed in temperate waters are the most Hg-contaminated species (the Amsterdam and Tristan albatrosses). These data emphasize the urgent need for robust assessment of the impact of Hg contamination on the biology of albatrosses and they document the high MeHg level exposure of wildlife living in the most remote marine areas on Earth.

Isolation and characterization of eight microsatellite loci from Galeocerdo cuvier (tiger shark) and cross-amplification in Carcharhinus leucas, Carcharhinus brevipinna, Carcharhinus plumbeus and Sphyrna lewini.

The tiger shark Galeocerdo cuvier (Carcharhinidae) is a large elasmobranch suspected to have, as other apex predators, a keystone function in marine ecosystems and is currently considered Near Threatened (Red list IUCN). Knowledge on its ecology, which is crucial to design proper conservation and management plans, is very scarce. Here we describe the isolation of eight polymorphic microsatellite loci using 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Their characteristics were tested on a population of tiger shark (n = 101) from Reunion Island (South-Western Indian Ocean). All loci were polymorphic with a number of alleles ranging from two to eight. No null alleles were detected and no linkage disequilibrium was detected after Bonferroni correction. Observed and expected heterozygosities ranged from 0.03 to 0.76 and from 0.03 to 0.77, respectively. No locus deviated from Hardy-Weinberg equilibrium and the global F IS of the population was of 0.04 (NS) . Some of the eight loci developed here successfully cross-amplified in the bull shark Carcharhinus leucas (one locus), the spinner shark Carcharhinus brevipinna (four loci), the sandbar shark Carcharhinus plumbeus (five loci) and the scalloped hammerhead shark Sphyrna lewini (two loci). We also designed primers to amplify and sequence a mitochondrial marker, the control region. We sequenced 862 bp and found a low genetic diversity, with four polymorphic sites, a haplotype diversity of 0.15 and a nucleotide diversity of 2 × 10(-4).

Combining Methods to Describe Important Marine Habitats for Top Predators: Application to Identify Biological Hotspots in Tropical Waters.

In tropical waters resources are usually scarce and patchy, and predatory species generally show specific adaptations for foraging. Tropical seabirds often forage in association with sub-surface predators that create feeding opportunities by bringing prey close to the surface, and the birds often aggregate in large multispecific flocks. Here we hypothesize that frigatebirds, a tropical seabird adapted to foraging with low energetic costs, could be a good predictor of the distribution of their associated predatory species, including other seabirds (e.g. boobies, terns) and subsurface predators (e.g., dolphins, tunas). To test this hypothesis, we compared distribution patterns of marine predators in the Mozambique Channel based on a long-term dataset of both vessel- and aerial surveys, as well as tracking data of frigatebirds. By developing species distribution models (SDMs), we identified key marine areas for tropical predators in relation to contemporaneous oceanographic features to investigate multi-species spatial overlap areas and identify predator hotspots in the Mozambique Channel. SDMs reasonably matched observed patterns and both static (e.g. bathymetry) and dynamic (e.g. Chlorophyll a concentration and sea surface temperature) factors were important explaining predator distribution patterns. We found that the distribution of frigatebirds included the distributions of the associated species. The central part of the channel appeared to be the best habitat for the four groups of species considered in this study (frigatebirds, brown terns, boobies and sub-surface predators).