Genomic insights into the historical and contemporary demographics of the grey reef shark.

Analyses of genetic diversity can shed light on both the origins of biodiversity hotspots, as well as the conservation status of species that are impacted by human activities. With these objectives, we assembled a genomic dataset of 14,935 single nucleotide polymorphisms from 513 grey reef sharks (Carcharhinus amblyrhynchos) sampled across 17 locations in the tropical Indo-Pacific. We analysed geographic variation in genetic diversity, estimated ancient and contemporary effective population size (Ne) across sampling locations (using coalescent and linkage disequilibrium methods) and modelled the history of gene flow between the Coral Triangle and the Coral Sea. Genetic diversity decreased with distance away from the Coral Triangle and north-western Australia, implying that C. amblyrhynchos may have originated in this region. Increases in Ne were detected across almost all sampling locations 40,000-90,000 generations ago (approximately 0.6-1.5 mya, given an estimated generation time of 16.4 years), suggesting a range expansion around this time. More recent, secondary increases in Ne were inferred for the Misool and North Great Barrier Reef sampling locations, but joint modelling did not clarify whether these were due to population growth, migration, or both. Despite the greater genetic diversity and ancient Ne observed at sites around Australia and the Coral Triangle, remote reefs around north-western New Caledonia had the highest contemporary Ne, demonstrating the importance of using multiple population size assessment methods. This study provides insight into both the past and present demographics of C. amblyrhynchos and contributes to our understanding of evolution in marine biodiversity hotspots.

Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes.

Ectotherms exhibit considerable plasticity in their life-history traits. This plasticity can reflect variability in environmental and social factors, but the causes of observed patterns are often obscured with increasing spatial scales. We surveyed dichromatic parrotfishes across the northern Great Barrier Reef to examine variation in body size distributions and concomitant size at sex change (L∆50 ) against hypotheses of directional influence from biotic and abiotic factors known to affect demography. By integrating top-down, horizontal, and bottom-up processes, we demonstrate a strong association between exposure regimes (which are known to influence nutritional ecology and mating systems) and both body size distribution and L∆50 (median length at female-to-male sex change), with an accompanying lack of strong empirical support for other biotic drivers previously hypothesized to affect body size distributions. Across sites, body size was predictably linked to variation in temperature and productivity, but the strongest predictor was whether subpopulations occurred at sheltered mid and inner shelf reefs or at wave-exposed outer shelf reef systems. Upon accounting for the underlying influence of body size distribution, this habitat-exposure gradient was highly associated with further L∆50 variation across species, demonstrating that differences in mating systems across exposure gradients affect the timing of sex change beyond variation concomitant with differing overall body sizes. We posit that exposure-driven differences in habitat disturbance regimes have marked effects on the nutritional ecology of parrotfishes, leading to size-related variation in mating systems, which underpin the observed patterns. Our results call for better integration of life-history, social factors, and ecosystem processes to foster an improved understanding of complex ecosystems such as coral reefs.

Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use.

Patterns of ecological specialization offer invaluable information about ecosystems. Yet, specialization is rarely quantified across several ecological niche axes and variables beyond the link between morphological and dietary specialization have received little attention. Here, we provide a quantitative evaluation of ecological specialization in a coral reef fish assemblage (f. Acanthuridae) along one fundamental and two realized niche axes. Specifically, we examined ecological specialization in 10 surgeonfish species with regards to morphology and two realized niche axes associated with diet and foraging microhabitat utilization using a recently developed multidimensional framework. We then investigated the potential relationships between morphological and behavioural specialization. These relationships differed markedly from the traditional ecomorphological paradigm. While morphological specialization showed no relationship with dietary specialization, it exhibited a strong relationship with foraging microhabitat specialization. However, this relationship was inverted: species with specialized morphologies were microhabitat generalists, whereas generalized morphotypes were microhabitat specialists. Interestingly, this mirrors relationships found in plant-pollinator communities and may also be applicable to other ecosystems, highlighting the potential importance of including niche axes beyond dietary specialization into ecomorphological frameworks. On coral reefs, it appears that morphotypes commonly perceived as most generalized may, in fact, be specialized in exploiting flat and easily accessible microhabitats.

Seascape effects on the nursery function of macroalgal habitats.

Understanding how seascape configuration influences nursery function is important for spatial management and conservation of essential habitats. Here, we examine how local habitat, seascape, and environmental factors influence demographic metrics of juvenile Lethrinus punctulatus and assess spatial variation in macroalgae nursery function. We quantified abundance, biomass, and productivity of juvenile L. punctulatus over three years and estimated size-at-age and condition from collected fish. Abundance, biomass, productivity, and size-at-age exhibited significant spatial variation, although each pattern was best explained by different factors. Lethrinus punctulatus were most abundant in macroalgae-rich seascapes, whereas biomass and productivity peaked where macroalgal cover and water temperatures were high. Conversely, fish exhibited the greatest average daily growth at sites near coral reefs. Processes contributing to spatial variation in size-at-age occur prior to fish reaching ∼5 cm in length and may be due to differences in resource availability, size at settlement, or size-selective mortality. Our findings suggest habitat and resource availability constrain L. punctulatus abundance and productivity, while size-at-age is influenced by size-selective mortality and prey quality. Thus, while seascape configuration can affect nursery function, the degree of influence will depend on the processes involved, emphasising the value of considering multiple metrics when identifying nurseries.

Recent expansion of marine protected areas matches with home range of grey reef sharks.

Dramatic declines in reef shark populations have been documented worldwide in response to human activities. Marine Protected Areas (MPAs) offer a useful mechanism to protect these species and their roles in coral reef ecosystems. The effectiveness of MPAs notably relies on compliance together with sufficient size to encompass animal home range. Here, we measured home range of 147 grey reef sharks, Carcharhinus amblyrhynchos, using acoustic telemetry in New Caledonia. The distribution of home range was then compared to local MPA sizes. We report a home range of 12 km2 of reef for the species with strong differences between adult males (21 km2), adult females (4.4 km2) and juveniles (6.2 km2 for males, 2.7 km2 for females). Whereas local historic MPA size seemed adequate to protect reef shark home range in general, these were clearly too small when considering adult males only, which is consistent with the reported failure of MPAs to protect sharks in New Caledonia. Fortunately, the recent implementation of several orders of magnitude larger MPAs in New Caledonia and abroad show that recent Indo-Pacific MPAs are now sufficiently large to protect the home ranges of this species, including males, across its geographical range. However, protection efforts are concentrated in a few regions and cannot provide adequate protection at a global scale.

Revisiting the paradigm of shark-driven trophic cascades in coral reef ecosystems.

Global overfishing of higher-level predators has caused cascading effects to lower trophic levels in many marine ecosystems. On coral reefs, which support highly diverse food webs, the degree to which top-down trophic cascades can occur remains equivocal. Using extensive survey data from coral reefs across the relatively unfished northern Great Barrier Reef (nGBR), we quantified the role of reef sharks in structuring coral reef fish assemblages. Using a structural equation modeling (SEM) approach, we explored the interactions between shark abundance and teleost mesopredator and prey functional group density and biomass, while explicitly accounting for the potentially confounding influence of environmental variation across sites. Although a fourfold difference in reef shark density was observed across our survey sites, this had no impact on either the density or biomass of teleost mesopredators or prey, providing evidence for a lack of trophic cascading across nGBR systems. Instead, many functional groups, including sharks, responded positively to environmental drivers. We found reef sharks to be positively associated with habitat complexity. In turn, physical processes such as wave exposure and current velocity were both correlated well with multiple functional groups, reflecting how changes to energetic conditions and food availability, or modification of habitat affect fish distribution. The diversity of species within coral reef food webs and their associations with bottom-up drivers likely buffers against trophic cascading across GBR functional guilds when reef shark assemblages are depleted, as has been demonstrated in other complex ecosystems.

Ongoing collapse of coral-reef shark populations.

Marine ecosystems are suffering severe depletion of apex predators worldwide; shark declines are principally due to conservative life-histories and fisheries overexploitation. On coral reefs, sharks are strongly interacting apex predators and play a key role in maintaining healthy reef ecosystems. Despite increasing fishing pressure, reef shark catches are rarely subject to specific limits, with management approaches typically depending upon no-take marine reserves to maintain populations. Here, we reveal that this approach is failing by documenting an ongoing collapse in two of the most abundant reef shark species on the Great Barrier Reef (Australia). We find an order of magnitude fewer sharks on fished reefs compared to no-entry management zones that encompass only 1% of reefs. No-take zones, which are more difficult to enforce than no-entry zones, offer almost no protection for shark populations. Population viability models of whitetip and gray reef sharks project ongoing steep declines in abundance of 7% and 17% per annum, respectively. These findings indicate that current management of no-take areas is inadequate for protecting reef sharks, even in one of the world's most-well-managed reef ecosystems. Further steps are urgently required for protecting this critical functional group from ecological extinction.

Environmental DNA illuminates the dark diversity of sharks.

In the era of "Anthropocene defaunation," large species are often no longer detected in habitats where they formerly occurred. However, it is unclear whether this apparent missing, or "dark," diversity of megafauna results from local species extirpations or from failure to detect elusive remaining individuals. We find that despite two orders of magnitude less sampling effort, environmental DNA (eDNA) detects 44% more shark species than traditional underwater visual censuses and baited videos across the New Caledonian archipelago (south-western Pacific). Furthermore, eDNA analysis reveals the presence of previously unobserved shark species in human-impacted areas. Overall, our results highlight a greater prevalence of sharks than described by traditional survey methods in both impacted and wilderness areas. This indicates an urgent need for large-scale eDNA assessments to improve monitoring of threatened and elusive megafauna. Finally, our findings emphasize the need for conservation efforts specifically geared toward the protection of elusive, residual populations.

Detecting conservation benefits of marine reserves on remote reefs of the northern GBR.

The Great Barrier Reef Marine Park (GBRMP) is the largest network of marine reserves in the world, yet little is known of the efficacy of no-fishing zones in the relatively lightly-exploited remote parts of the system (i.e., northern regions). Here, we find that the detection of reserve effects is challenging and that heterogeneity in benthic habitat composition, specifically branching coral cover, is one of the strongest driving forces of fish assemblages. As expected, the biomass of targeted fish species was generally greater (up to 5-fold) in no-take zones than in fished zones, but we found no differences between the two forms of no-take zone: 'no-take' versus 'no-entry'. Strong effects of zoning were detected in the remote Far-North inshore reefs and more central outer reefs, but surprisingly fishing effects were absent in the less remote southern locations. Moreover, the biomass of highly targeted species was nearly 2-fold greater in fished areas of the Far-North than in any reserve (no-take or no-entry) further south. Despite high spatial variability in fish biomass, our results suggest that fishing pressure is greater in southern areas and that poaching within reserves may be common. Our results also suggest that fishers 'fish the line' as stock sizes in exploited areas decreased near larger no-take zones. Interestingly, an analysis of zoning effects on small, non-targeted fishes appeared to suggest a top-down effect from mesopredators, but was instead explained by variability in benthic composition. Thus, we demonstrate the importance of including appropriate covariates when testing for evidence of trophic cascades and reserve successes or failures.

Connectivity in grey reef sharks (Carcharhinus amblyrhynchos) determined using empirical and simulated genetic data.

Grey reef sharks (Carcharhinus amblyrhynchos) can be one of the numerically dominant high order predators on pristine coral reefs, yet their numbers have declined even in the highly regulated Australian Great Barrier Reef (GBR) Marine Park. Knowledge of both large scale and fine scale genetic connectivity of grey reef sharks is essential for their effective management, but no genetic data are yet available. We investigated grey reef shark genetic structure in the GBR across a 1200 km latitudinal gradient, comparing empirical data with models simulating different levels of migration. The empirical data did not reveal any genetic structuring along the entire latitudinal gradient sampled, suggesting regular widespread dispersal and gene flow of the species throughout most of the GBR. Our simulated datasets indicate that even with substantial migrations (up to 25% of individuals migrating between neighboring reefs) both large scale genetic structure and genotypic spatial autocorrelation at the reef scale were maintained. We suggest that present migration rates therefore exceed this level. These findings have important implications regarding the effectiveness of networks of spatially discontinuous Marine Protected Areas to protect reef sharks.

Experimental evaluation of shark detection rates by aerial observers.

Aerial surveys are a recognised technique to identify the presence and abundance of marine animals. However, the capability of aerial observers to reliably sight coastal sharks has not been previously assessed, nor have differences in sighting rates between aircraft types been examined. In this study we investigated the ability of observers in fixed-wing and helicopter aircraft to sight 2.5 m artificial shark analogues placed at known depths and positions. Initial tests revealed that the shark analogues could only be detected at shallow depths, averaging only 2.5 m and 2.7 m below the water surface for observers in fixed-wing and helicopter aircraft, respectively. We then deployed analogues at shallower depths along a 5 km-long grid, and assessed their sightability to aircraft observers through a series of transects flown within 500 m. Analogues were seen infrequently from all distances, with overall sighting rates of only 12.5% and 17.1% for fixed-wing and helicopter observers, respectively. Although helicopter observers had consistently higher success rates of sighting analogues within 250 m of their flight path, neither aircraft observers sighted more than 9% of analogues deployed over 300 m from their flight paths. Modelling of sighting rates against environmental and experimental variables indicated that observations were affected by distance, aircraft type, sun glare and sea conditions, while the range of water turbidities observed had no effect. We conclude that aerial observers have limited ability to detect the presence of submerged animals such as sharks, particularly when the sharks are deeper than ∼ 2.6 m, or over 300 m distant from the aircraft's flight path, especially during sunny or windy days. The low rates of detections found in this study cast serious doubts on the use of aerial beach patrols as an effective early-warning system to prevent shark attacks.

Population growth rates of reef sharks with and without fishing on the great barrier reef: robust estimation with multiple models.

Overfishing of sharks is a global concern, with increasing numbers of species threatened by overfishing. For many sharks, both catch rates and underwater visual surveys have been criticized as indices of abundance. In this context, estimation of population trends using individual demographic rates provides an important alternative means of assessing population status. However, such estimates involve uncertainties that must be appropriately characterized to credibly and effectively inform conservation efforts and management. Incorporating uncertainties into population assessment is especially important when key demographic rates are obtained via indirect methods, as is often the case for mortality rates of marine organisms subject to fishing. Here, focusing on two reef shark species on the Great Barrier Reef, Australia, we estimated natural and total mortality rates using several indirect methods, and determined the population growth rates resulting from each. We used bootstrapping to quantify the uncertainty associated with each estimate, and to evaluate the extent of agreement between estimates. Multiple models produced highly concordant natural and total mortality rates, and associated population growth rates, once the uncertainties associated with the individual estimates were taken into account. Consensus estimates of natural and total population growth across multiple models support the hypothesis that these species are declining rapidly due to fishing, in contrast to conclusions previously drawn from catch rate trends. Moreover, quantitative projections of abundance differences on fished versus unfished reefs, based on the population growth rate estimates, are comparable to those found in previous studies using underwater visual surveys. These findings appear to justify management actions to substantially reduce the fishing mortality of reef sharks. They also highlight the potential utility of rigorously characterizing uncertainty, and applying multiple assessment methods, to obtain robust estimates of population trends in species threatened by overfishing.