Retrospective genomics highlights changes in genetic composition of tiger sharks (Galeocerdo cuvier) and potential loss of a south-eastern Australia population.

Over the last century, many shark populations have declined, primarily due to overexploitation in commercial, artisanal and recreational fisheries. In addition, in some locations the use of shark control programs also has had an impact on shark numbers. Still, there is a general perception that populations of large ocean predators cover wide areas and therefore their diversity is less susceptible to local anthropogenic disturbance. Here we report on temporal genomic analyses of tiger shark (Galeocerdo cuvier) DNA samples that were collected from eastern Australia over the past century. Using Single Nucleotide Polymorphism (SNP) loci, we documented a significant change in genetic composition of tiger sharks born between ~1939 and 2015. The change was most likely due to a shift over time in the relative contribution of two well-differentiated, but hitherto cryptic populations. Our data strongly indicate a dramatic shift in the relative contribution of these two populations to the overall tiger shark abundance on the east coast of Australia, possibly associated with differences in direct or indirect exploitation rates.

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.

Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator.

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.

Lack of multiple paternity in the oceanodromous tiger shark (Galeocerdo cuvier).

Multiple paternity has been documented as a reproductive strategy in both viviparous and ovoviviparous elasmobranchs, leading to the assumption that multiple mating may be ubiquitous in these fishes. However, with the majority of studies conducted on coastal and nearshore elasmobranchs that often form mating aggregations, parallel studies on pelagic, semi-solitary species are lacking. The tiger shark (Galeocerdo cuvier) is a large pelagic shark that has an aplacental viviparous reproductive mode which is unique among the carcharhinids. A total of 112 pups from four pregnant sharks were genotyped at nine microsatellite loci to assess the possibility of multiple paternity or polyandrous behaviour by female tiger sharks. Only a single pup provided evidence of possible multiple paternity, but with only seven of the nine loci amplifying for this individual, results were inconclusive. In summary, it appears that the tiger sharks sampled in this study were genetically monogamous. These findings may have implications for the genetic diversity and future sustainability of this population.

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.

Population structure and connectivity of tiger sharks (Galeocerdo cuvier) across the Indo-Pacific Ocean basin.

Population genetic structure using nine polymorphic nuclear microsatellite loci was assessed for the tiger shark (Galeocerdo cuvier) at seven locations across the Indo-Pacific, and one location in the southern Atlantic. Genetic analyses revealed considerable genetic structuring (FST > 0.14, p < 0.001) between all Indo-Pacific locations and Brazil. By contrast, no significant genetic differences were observed between locations from within the Pacific or Indian Oceans, identifying an apparent large, single Indo-Pacific population. A lack of differentiation between tiger sharks sampled in Hawaii and other Indo-Pacific locations identified herein is in contrast to an earlier global tiger shark nDNA study. The results of our power analysis provide evidence to suggest that the larger sample sizes used here negated any weak population subdivision observed previously. These results further highlight the need for cross-jurisdictional efforts to manage the sustainable exploitation of large migratory sharks like G. cuvier.

Environmental influences and ontogenetic differences in vertical habitat use of black marlin (Istiompax indica) in the southwestern Pacific.

The black marlin (Istiompax indica) is a highly migratory billfish that occupies waters throughout the tropical and subtropical Indo-Pacific. To characterize the vertical habitat use of I. indica, we examined the temperature-depth profiles collected using 102 pop-up satellite archival tags deployed off the east coast of Australia. Modelling of environmental variables revealed location, sea-surface height deviation, mixed layer depth and dissolved oxygen to all be significant predictors of vertical habitat use. Distinct differences in diel movements were observed between the size classes, with larger size classes of marlin (greater than 50 kg) undertaking predictable bounce-diving activity during daylight hours, while diving behaviour of the smallest size class occurred randomly during both day and night. Overall, larger size classes of I. indica were found to use an increased thermal range and spend more time in waters below 150 m than fish of smaller size classes. The differences in the diving behaviour among size classes were suggested to reflect ontogenetic differences in foraging behaviour or physiology. The findings of this study demonstrate, for the first time to our knowledge, ontogenetic differences in vertical habitat in a species of billfish, and further the understanding of pelagic fish ecophysiology in the presence of global environmental change.

The Novel Application of Non-Lethal Citizen Science Tissue Sampling in Recreational Fisheries.

Increasing fishing pressure and uncertainty surrounding recreational fishing catch and effort data promoted the development of alternative methods for conducting fisheries research. A pilot investigation was undertaken to engage the Australian game fishing community and promote the non-lethal collection of tissue samples from the black marlin Istiompax indica, a valuable recreational-only species in Australian waters, for the purpose of future genetic research. Recruitment of recreational anglers was achieved by publicizing the project in magazines, local newspapers, social media, blogs, websites and direct communication workshops at game fishing tournaments. The Game Fishing Association of Australia and the Queensland Game Fishing Association were also engaged to advertise the project and recruit participants with a focus on those anglers already involved in the tag-and-release of marlin. Participants of the program took small tissue samples using non-lethal methods which were stored for future genetic analysis. The program resulted in 165 samples from 49 participants across the known distribution of I. indica within Australian waters which was a sufficient number to facilitate a downstream population genetic analysis. The project demonstrated the potential for the development of citizen science sampling programs to collect tissue samples using non-lethal methods in order to achieve targeted research objects in recreationally caught species.