A global perspective on the trophic geography of sharks.

Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.

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.

Larval fish dispersal in a coral-reef seascape.

Larval dispersal is a critical yet enigmatic process in the persistence and productivity of marine metapopulations. Empirical data on larval dispersal remain scarce, hindering the use of spatial management tools in efforts to sustain ocean biodiversity and fisheries. Here we document dispersal among subpopulations of clownfish (Amphiprion percula) and butterflyfish (Chaetodon vagabundus) from eight sites across a large seascape (10,000 km2) in Papua New Guinea across 2 years. Dispersal of clownfish was consistent between years, with mean observed dispersal distances of 15 km and 10 km in 2009 and 2011, respectively. A Laplacian statistical distribution (the dispersal kernel) predicted a mean dispersal distance of 13-19 km, with 90% of settlement occurring within 31-43 km. Mean dispersal distances were considerably greater (43-64 km) for butterflyfish, with kernels declining only gradually from spawning locations. We demonstrate that dispersal can be measured on spatial scales sufficient to inform the design of and test the performance of marine reserve networks.

A test of trophic cascade theory: fish and benthic assemblages across a predator density gradient on coral reefs.

Removal of predators is often hypothesized to alter community structure through trophic cascades. However, despite recent advances in our understanding of trophic cascades, evidence is often circumstantial on coral reefs because fishing pressure frequently co-varies with other anthropogenic effects, such as fishing for herbivorous fishes and changes in water quality due to pollution. Australia's outer Great Barrier Reef (GBR) has experienced fishing-induced declines of apex predators and mesopredators, but pollution and targeting of herbivorous fishes are minimal. Here, we quantify fish and benthic assemblages across a fishing-induced predator density gradient on the outer GBR, including apex predators and mesopredators to herbivores and benthic assemblages, to test for evidence of trophic cascades and alternative hypotheses to trophic cascade theory. Using structural equation models, we found no cascading effects from apex predators to lower trophic levels: a loss of apex predators did not lead to higher levels of mesopredators, and this did not suppress mobile herbivores and drive algal proliferation. Likewise, we found no effects of mesopredators on lower trophic levels: a decline of mesopredators was not associated with higher abundances of algae-farming damselfishes and algae-dominated reefs. These findings indicate that top-down forces on coral reefs are weak, at least on the outer GBR. We conclude that predator-mediated trophic cascades are probably the exception rather than the rule in complex ecosystems such as the outer GBR.

Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park.

Larval dispersal is the key process by which populations of most marine fishes and invertebrates are connected and replenished. Advances in larval tagging and genetics have enhanced our capacity to track larval dispersal, assess scales of population connectivity, and quantify larval exchange among no-take marine reserves and fished areas. Recent studies have found that reserves can be a significant source of recruits for populations up to 40 km away, but the scale and direction of larval connectivity across larger seascapes remain unknown. Here, we apply genetic parentage analysis to investigate larval dispersal patterns for two exploited coral reef groupers (Plectropomus maculatus and Plectropomus leopardus) within and among three clusters of reefs separated by 60-220 km within the Great Barrier Reef Marine Park, Australia. A total of 69 juvenile P. maculatus and 17 juvenile P. leopardus (representing 6% and 9% of the total juveniles sampled, respectively) were genetically assigned to parent individuals on reefs within the study area. We identified both short-distance larval dispersal within regions (200 m to 50 km) and long-distance, multidirectional dispersal of up to ~250 km among regions. Dispersal strength declined significantly with distance, with best-fit dispersal kernels estimating median dispersal distances of ~110 km for P. maculatus and ~190 km for P. leopardus. Larval exchange among reefs demonstrates that established reserves form a highly connected network and contribute larvae for the replenishment of fished reefs at multiple spatial scales. Our findings highlight the potential for long-distance dispersal in an important group of reef fishes, and provide further evidence that effectively protected reserves can yield recruitment and sustainability benefits for exploited fish populations.

The role of marine reserves in the replenishment of a locally impacted population of anemonefish on the Great Barrier Reef.

The development of parentage analysis to track the dispersal of juvenile offspring has given us unprecedented insight into the population dynamics of coral reef fishes. These tools now have the potential to inform fisheries management and species conservation, particularly for small fragmented populations under threat from exploitation and disturbance. In this study, we resolve patterns of larval dispersal for a population of the anemonefish Amphiprion melanopus in the Keppel Islands (southern Great Barrier Reef). Habitat loss and fishing appear to have impacted this population and a network of no-take marine reserves currently protects 75% of the potential breeders. Using parentage analysis, we estimate that 21% of recruitment in the island group was generated locally and that breeding adults living in reserves were responsible for 79% (31 of 39) of these of locally produced juveniles. Overall, the network of reserves was fully connected via larval dispersal; however, one reserve was identified as a critical source of larvae for the island group. The population in the Keppel Islands also appears to be well-connected to other source populations at least 60 km away, given that 79% (145 of 184) of the juveniles sampled remained unassigned in the parentage analysis. We estimated the effective size of the A. melanopus metapopulation to be 745 (582-993 95% CI) and recommend continued monitoring of its genetic status. Maintaining connectivity with populations beyond the Keppel Islands and recovery of local recruitment habitat, potentially through active restoration of host anemone populations, will be important for its long-term persistence.

Selective Impact of Disease on Coral Communities: Outbreak of White Syndrome Causes Significant Total Mortality of Acropora Plate Corals.

Coral diseases represent a significant and increasing threat to coral reefs. Among the most destructive diseases is White Syndrome (WS), which is increasing in distribution and prevalence throughout the Indo-Pacific. The aim of this study was to determine taxonomic and spatial patterns in mortality rates of corals following the 2008 outbreak of WS at Christmas Island in the eastern Indian Ocean. WS mainly affected Acropora plate corals and caused total mortality of 36% of colonies across all surveyed sites and depths. Total mortality varied between sites but was generally much greater in the shallows (0-96% of colonies at 5 m depth) compared to deeper waters (0-30% of colonies at 20 m depth). Site-specific mortality rates were a reflection of the proportion of corals affected by WS at each site during the initial outbreak and were predicted by the initial cover of live Acropora plate cover. The WS outbreak had a selective impact on the coral community. Following the outbreak, live Acropora plate coral cover at 5 m depth decreased significantly from 7.0 to 0.8%, while the cover of other coral taxa remained unchanged. Observations five years after the initial outbreak revealed that total Acropora plate cover remained low and confirmed that corals that lost all their tissue due to WS did not recover. These results demonstrate that WS represents a significant and selective form of coral mortality and highlights the serious threat WS poses to coral reefs in the Indo-Pacific.

Impact of conservation areas on trophic interactions between apex predators and herbivores on coral reefs.

Apex predators are declining at alarming rates due to exploitation by humans, but we have yet to fully discern the impacts of apex predator loss on ecosystem function. In a management context, it is critically important to clarify the role apex predators play in structuring populations of lower trophic levels. Thus, we examined the top-down influence of reef sharks (an apex predator on coral reefs) and mesopredators on large-bodied herbivores. We measured the abundance, size structure, and biomass of apex predators, mesopredators, and herbivores across fished, no-take, and no-entry management zones in the Great Barrier Reef Marine Park, Australia. Shark abundance and mesopredator size and biomass were higher in no-entry zones than in fished and no-take zones, which indicates the viability of strictly enforced human exclusion areas as tools for the conservation of predator communities. Changes in predator populations due to protection in no-entry zones did not have a discernible influence on the density, size, or biomass of different functional groups of herbivorous fishes. The lack of a relationship between predators and herbivores suggests that top-down forces may not play a strong role in regulating large-bodied herbivorous coral reef fish populations. Given this inconsistency with traditional ecological theories of trophic cascades, trophic structures on coral reefs may need to be reassessed to enable the establishment of appropriate and effective management regimes.

Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes.

BACKGROUND: Rising sea temperatures are causing significant destruction to coral reef ecosystems due to coral mortality from thermally-induced bleaching (loss of symbiotic algae and/or their photosynthetic pigments). Although bleaching has been intensively studied in corals, little is known about the causes and consequences of bleaching in other tropical symbiotic organisms. METHODOLOGY/PRINCIPAL FINDINGS: This study used underwater visual surveys to investigate bleaching in the 10 species of anemones that host anemonefishes. Bleaching was confirmed in seven anemone species (with anecdotal reports of bleaching in the other three species) at 10 of 19 survey locations spanning the Indo-Pacific and Red Sea, indicating that anemone bleaching is taxonomically and geographically widespread. In total, bleaching was observed in 490 of the 13,896 surveyed anemones (3.5%); however, this percentage was much higher (19-100%) during five major bleaching events that were associated with periods of elevated water temperatures and coral bleaching. There was considerable spatial variation in anemone bleaching during most of these events, suggesting that certain sites and deeper waters might act as refuges. Susceptibility to bleaching varied between species, and in some species, bleaching caused reductions in size and abundance. CONCLUSIONS/SIGNIFICANCE: Anemones are long-lived with low natural mortality, which makes them particularly vulnerable to predicted increases in severity and frequency of bleaching events. Population viability will be severely compromised if anemones and their symbionts cannot acclimate or adapt to rising sea temperatures. Anemone bleaching also has negative effects to other species, particularly those that have an obligate relationship with anemones. These effects include reductions in abundance and reproductive output of anemonefishes. Therefore, the future of these iconic and commercially valuable coral reef fishes is inextricably linked to the ability of host anemones to cope with rising sea temperatures associated with climate change.

Effects of spearfishing on reef fish populations in a multi-use conservation area.

Although spearfishing is a popular method of capturing fish, its ecological effects on fish populations are poorly understood, which makes it difficult to assess the legitimacy and desirability of spearfishing in multi-use marine reserves. Recent management changes within the Great Barrier Reef Marine Park (GBRMP) fortuitously created a unique scenario by which to quantify the effects of spearfishing on fish populations. As such, we employed underwater visual surveys and a before-after-control-impact experimental design to investigate the effects of spearfishing on the density and size structure of target and non-target fishes in a multi-use conservation park zone (CPZ) within the GBRMP. Three years after spearfishing was first allowed in the CPZ, there was a 54% reduction in density and a 27% reduction in mean size of coral trout (Plectropomus spp.), the primary target species. These changes were attributed to spearfishing because benthic habitat characteristics and the density of non-target fishes were stable through time, and the density and mean size of coral trout in a nearby control zone (where spearfishing was prohibited) remained unchanged. We conclude that spearfishing, like other forms of fishing, can have rapid and substantial negative effects on target fish populations. Careful management of spearfishing is therefore needed to ensure that conservation obligations are achieved and that fishery resources are harvested sustainably. This is particularly important both for the GBRMP, due to its extraordinarily high conservation value and world heritage status, and for tropical island nations where people depend on spearfishing for food and income. To minimize the effects of spearfishing on target species and to enhance protection of functionally important fishes (herbivores), we recommend that fishery managers adjust output controls such as size- and catch-limits, rather than prohibit spearfishing altogether. This will preserve the cultural and social importance of spearfishing in coastal communities where it is practised.

Coral disease in the Indian Ocean: taxonomic susceptibility, spatial distribution and the role of host density on the prevalence of white syndrome.

Coral diseases, such as white diseases and white syndrome (WS), have caused widespread damage to coral reefs throughout the Caribbean and are increasing in prevalence on Pacific Ocean reefs. The current study confirms that WS is also present on coral reefs in the Indian Ocean and tests whether patterns in taxonomic susceptibility and spatial variability conform to patterns of WS reported in the Pacific Ocean. Underwater surveys at 19 sites around Christmas and Cocos Islands revealed that WS primarily affects Acropora plate corals (A. clathrata, A. cytherea and A. hyacinthus), and prevalence of WS varied significantly across all 3 spatial scales investigated (island, exposure and depth). Approximately 13.0% (range = 0 to 43% per site) of plate corals at Christmas Island sites exhibited WS compared to <1% at the Cocos Islands. At Christmas Island, WS prevalence was greater in shallow (31.5%) than in deeper water (6.7%) and greatest on the northern (leeward) side of the island (31.5%) compared to the more exposed coastlines (0 to 1.5%). Importantly, the spatial distribution of WS was positively correlated with host density, but not with hard coral cover, suggesting a role of host density in WS outbreaks. Overall the present study has established that WS is impacting remote, near-pristine reefs in the Indian Ocean. However, the highly variable spatial distribution of WS illustrates that patterns in disease prevalence, and the subsequent impact on coral reefs, can be location- or region-specific.

Marine hybrid hotspot at Indo-Pacific biogeographic border.

Studying hybridization is crucial to understanding speciation and almost all our knowledge comes from terrestrial and freshwater environments. Marine hybrids are considered rare, particularly on species-rich coral reefs. Here, we report a significant marine hybrid zone at Christmas and Cocos Islands (eastern Indian Ocean) with 11 hybrid coral reef fishes (across six families); the most recorded hybrids of any marine location. In most cases, at least one of the parent species is rare (less than three individuals per 3000 m(2)), suggesting that hybridization has occurred because individuals of the rare species have mated with another species owing to a scarcity of conspecific partners. These islands also represent a marine suture zone where many of the hybrids have arisen through interbreeding between Indian and Pacific Ocean species. For these species, it appears that past climate changes allowed species to diverge in allopatry, while recent conditions have facilitated contact and subsequent hybridization at this Indo-Pacific biogeographic border. The discovery of the Christmas-Cocos hybrid zone refutes the notion that hybridization is lacking on coral reefs and provides a natural laboratory for testing the generality of terrestrially derived hybridization theory in the marine environment.