Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Author Correction: DNA-based identification of predators of the corallivorous Crown-of-Thorns Starfish (Acanthaster cf. solaris) from fish faeces and gut contents.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Relative efficacy of three approaches to mitigate Crown-of-Thorns Starfish outbreaks on Australia's Great Barrier Reef.

Population outbreaks of Crown-of-Thorns Starfish (COTS; Acanthaster spp.) are a major contributor to loss of hard coral throughout the Indo-Pacific. On Australia's Great Barrier Reef (GBR), management interventions have evolved over four COTS outbreaks to include: (1) manual COTS control, (2) Marine Protected Area (MPA) zoning, and, (3) water quality improvement. Here we evaluate the contribution of these three approaches to managing population outbreaks of COTS to minimize coral loss. Strategic manual control at sites reduced COTS numbers, including larger, more fecund and damaging individuals. Sustained reduction in COTS densities and improvements in hard coral cover at a site were achieved through repeated control visits. MPAs influenced initial COTS densities but only marginally influenced final hard coral cover following COTS control. Water quality improvement programs have achieved only marginal reductions in river nutrient loads delivered to the GBR and the study region. This, a subsequent COTS outbreak, and declining coral cover across the region suggest their contributions are negligible. These findings support manual control as the most direct, and only effective, means of reducing COTS densities and improving hard coral cover currently available at a site. We provide recommendations for improving control program effectiveness with application to supporting reef resilience across the Indo-Pacific.

DNA-based identification of predators of the corallivorous Crown-of-Thorns Starfish (Acanthaster cf. solaris) from fish faeces and gut contents.

The corallivorous Crown-of-Thorns Starfish (CoTS, Acanthaster spp.) has been linked with the widespread loss of scleractinian coral cover on Indo-Pacific reefs during periodic population outbreaks. Here, we re-examine CoTS consumption by coral reef fish species by using new DNA technologies to detect Pacific Crown-of-Thorns Starfish (Acanthaster cf. solaris) in fish faecal and gut content samples. CoTS DNA was detected in samples from 18 different coral reef fish species collected on reefs at various stages of CoTS outbreaks in the Great Barrier Reef Marine Park, nine of which had not been previously reported to feed on CoTS. A comprehensive set of negative and positive control samples confirmed that our collection, processing and analysis procedures were robust, although food web transfer of CoTS DNA cannot be ruled out for some fish species. Our results, combined with the (i) presence of CoTS spines in some samples, (ii) reported predation on CoTS gametes, larvae and settled individuals, and (iii) known diet information for fish species examined, strongly indicate that direct fish predation on CoTS may well be more common than is currently appreciated. We provide recommendations for specific management approaches to enhance predation on CoTS by coral reef fishes, and to support the mitigation of CoTS outbreaks and reverse declines in hard coral cover.

Loss of live coral compromises predator-avoidance behaviour in coral reef damselfish.

Tropical reefs have experienced an unprecedented loss of live coral in the past few decades and the biodiversity of coral-dependent species is under threat. Many reef fish species decline in abundance as coral cover is lost, yet the mechanisms responsible for these losses are largely unknown. A commonly hypothesised cause of fish decline is the loss of shelter space between branches as dead corals become overgrown by algae. Here we tested this hypothesis by quantifying changes in predator-avoidance behaviour of a common damselfish, Pomacentrus moluccensis, before and after the death of their coral colony. Groups of P. moluccensis were placed on either healthy or degraded coral colonies, startled using a visual stimulus and their sheltering responses compared over a 7-week period. P. moluccensis stopped sheltering amongst the coral branches immediately following the death of the coral, despite the presence of ample shelter space. Instead, most individuals swam away from the dead coral, potentially increasing their exposure to predators. It appears that the presence of live coral rather than shelter per se is the necessary cue that elicits the appropriate behavioural response to potential predators. The disruption of this link poses an immediate threat to coral-associated fishes on degrading reefs.

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.

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.

Contrasting effects of habitat loss and fragmentation on coral-associated reef fishes.

Disturbance can result in the fragmentation and/or loss of suitable habitat, both of which can have important consequences for survival, species interactions, and resulting patterns of local diversity. However, effects of habitat loss and fragmentation are typically confounded during disturbance events, and previous attempts to determine their relative significance have proved ineffective. Here we experimentally manipulated live coral habitats to examine the potential independent and interactive effects of habitat loss and fragmentation on survival, abundance, and species richness of recruitment-stage, coral-associated reef fishes. Loss of 75% of live coral from experimental reefs resulted in low survival of a coral-associated damselfish and low abundance and richness of other recruits 16 weeks after habitat manipulations. In contrast, fragmentation had positive effects on damselfish survival and resulted in greater abundance and species richness of other recruits. We hypothesize that spacing of habitat through fragmentation weakens competition within and among species. Comparison of effect sizes over the course of the study period revealed that, in the first six weeks following habitat manipulations, the positive effects of fragmentation were at least four times stronger than the effects of habitat loss. This initial positive effect of fragmentation attenuated considerably after 16 weeks, whereas the negative effects of habitat loss increased in strength over time. There was little indication that the amount of habitat influenced the magnitude of the habitat fragmentation effect. Numerous studies have reported dramatic declines in coral reef fish abundance and diversity in response to disturbances that cause the loss and fragmentation of coral habitats. Our results suggest that these declines occur as a result of habitat loss, not habitat fragmentation. Positive fragmentation effects may actually buffer against the negative effects of habitat loss and contribute to the resistance of reef fish populations to declines in coral cover.