William D. Robbins

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 worlds most-well-managed reef ecosystems. Further steps are urgently required for protecting this critical functional group from ecological extinction.

Decadal trends in shark catches and effort from the New South Wales, Australia, Shark Meshing Program 1950-2010

The New South Wales (NSW) government has operated a program of netting beaches for the protection of swimmers and surfers against shark attack since 1937 in Sydney, and since 1949 in Newcastle and Wollongong. The scope and directives of the Shark Meshing Program have remained constant since its inception, with operational modifications in net specifications in 1972, changes in spatial deployment in 1972, 1987 and 1992, and the elimination of winter netting since 1989. This markedly increased meshing effort in 1972, and again in 1987. In the present study, we examine the trends in catch and effort for the period from 1950–1951 to 2009–2010 over this 200-km section of the NSW coast. Significant temporal trends in species, size and sex composition are described herein. Catches were consistently dominated by three shark taxa, hammerhead sharks (Sphyrna spp.), whaler sharks (Carcharhinus spp.) and Australian angel sharks (Squatina australis), although their relative contributions to catches varied over time. Catch per unit effort has significantly declined for five of the most abundant shark taxa over the study period, increasing only for a single taxon, the sevengill shark (Notorynchus cepedianus). Catches of larger, potentially dangerous white sharks (Carcharodon carcharias) and tiger sharks (Galeocerdo cuvier) saw fewer large animals being caught over time. This pattern was not observed across other taxa. Four different monthly trends were observed in landings of the most abundant eight taxa, reflecting differences in the biology of the catch species. The current study also provides useful information on catches and sizes of grey nurse (Carcharias taurus) and white sharks before and after their protection in NSW waters in 1984 and 1998, respectively.

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.

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.

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 aircrafts 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.

Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos)

With overfishing reducing the abundance of marine predators in multiple marine ecosystems, knowledge of genetic structure and local adaptation may provide valuable information to assist sustainable management. Despite recent technological advances, most studies on sharks have used small sets of neutral markers to describe their genetic structure. We used 5517 nuclear single-nucleotide polymorphisms (SNPs) and a mitochondrial DNA (mtDNA) gene to characterize patterns of genetic structure and detect signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Using samples from Australia, Indonesia and oceanic reefs in the Indian Ocean, we established that large oceanic distances represent barriers to gene flow, whereas genetic differentiation on continental shelves follows an isolation by distance model. In Australia and Indonesia differentiation at nuclear SNPs was weak, with coral reefs acting as stepping stones maintaining connectivity across large distances. Differentiation of mtDNA was stronger, and more pronounced in females, suggesting sex-biased dispersal. Four independent tests identified a set of loci putatively under selection, indicating that grey reef sharks in eastern Australia are likely under different selective pressures to those in western Australia and Indonesia. Genetic distances averaged across all loci were uncorrelated with genetic distances calculated from outlier loci, supporting the conclusion that different processes underpin genetic divergence in these two data sets. This pattern of heterogeneous genomic differentiation, suggestive of local adaptation, has implications for the conservation of grey reef sharks; furthermore, it highlights that marine species showing little genetic differentiation at neutral loci may exhibit patterns of cryptic genetic structure driven by local selection.

Characterisation of 15 novel microsatellite loci for the grey reef shark (Carcharhinus amblyrhynchos)

AbstractGrey reef sharks (Carcharhinus amblyrhynchos) are important apex predators on coral reefs, and their numbers have declined dramatically as a result of overfishing. Knowledge of environmental factors that shape gene flow is essential for developing appropriate management strategies, but the lack of suitable genetic markers has hindered research on this species. Here, we characterised 15 polymorphic microsatellite loci for grey reef sharks. None of the loci deviated significantly from Hardy–Weinberg equilibrium and there was no evidence of Linkage Disequilibrium. Several loci cross-amplified in other carcharhinid species, and will be useful in future studies of this family.

A multifaceted approach to modelling growth of the Australian bonito, Sarda australis (Family Scombridae), with some observations on its reproductive biology

Growth of the Australian bonito, Sarda australis, is described for the first time using data from three different sources. Von Bertalanffy growth functions were fitted to: (1) size-at-age data derived from sectioned sagittal otoliths, (2) monthly length–frequency collections from a commercial line fishery, and (3) tag–recapture data from a long-term cooperative tagging study. Age estimates of S. australis were indirectly validated by examining the percentage of otoliths with opaque edges each month. The best-fitting growth functions for each data source yielded similar results, showing strong seasonal variations in growth rate. Maximum growth occurred during summer, with near cessation of growth apparent during winter. Early growth was very fast, with fish attaining ~30 cm fork length (FL) after 3–4 months. Growth of males and females was not significantly different. The oldest fish sampled was estimated to be 3+ years old, while the largest fish aged was 63.8 cm FL. Gonadosomatic indices indicated that S. australis has an austral spring/summer spawning period in eastern Australia. A preliminary estimate of the size at first sexual maturity was ~36 cm FL for both males and females, corresponding to an age of ~1 year.

Reef sharks clean up with a novel inshore mutualistic interaction

Parasite removal by cleaner fish provides significant health benefits to a variety of coral reef fish, particularly roving carnivores and herbivores (Grutter et al. 2003). For grey reef sharks (Carcharhinus amblyrhynchos), however, such cleaning events are only known to occur sporadically, on exposed oceanic reefs (O’Shea et al. 2010). This is because hosts on cleaning stations must remain relatively stationary (Côté et al. 1998), a behaviour which requires constant current flow for grey reef sharks. Within the central region of Ningaloo Reef (S 23.1, E 113.8), an 8-mdeep lagoonal Turbinaria coral bommie provides the only reported example of grey reef sharks utilising a shallow-water inshore cleaner fish station (Fig. 1a). Here, sharks of both sexes up to 1.8 m total length are cleaned by blue-streak cleaner wrasse (Labroides dimidiatus) and moon wrasse (Thalassoma lunare). Analysis of remote video footage revealed as many as 18 grey reef sharks circle the area surrounding the cleaning station (~325 m), with up to 12 individuals being cleaned simultaneously on the 6-m wide bommie. Cleaning interactions are initiated by the sharks, which face into the prevailing current, adopting a vertical posture (Fig. 1b; O’Shea et al. 2010). Grey reef shark abundance and the number of cleaning interactions increase with current strength for all but the highest velocities (S. Wheeler pers obs). These observations were made during 31 days of surveying over a 3-month period, although grey reef shark cleaning interactions were consistently observed during the 11 months prior (approximately 5 days per week). We did not sight other shark species using the cleaning station, although they are present at Ningaloo Reef. We suggest the particular combination of water depth, and consistently high current flow facilitates the use of this inshore reef cleaning station by grey reef sharks. The steady current provides the sharks with a mechanism to hover and fulfil their oxygen demands, while the convoluted Turbinaria coral proffers the cleaner wrasses ideal habitat for shelter. This location confers a unique opportunity to study the only wild interaction recorded between coral reef sharks and labrid fishes outside of exposed oceanic reefs. Given the large number of sharks that regularly aggregate at the site, it also forms the focus of a growing dive tourism industry.