Predation on the early life stages of the crown-of-thorns starfish (Acanthaster cf. solaris)

Cowan, Zara-Louise (2017) Predation on the early life stages of the crown-of-thorns starfish (Acanthaster cf. solaris). PhD thesis, James Cook University.

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Population outbreaks of crown-of-thorns starfish (CoTS, Acanthaster spp.) represent one of the most significant biological disturbances on tropical reefs, contributing to widespread and significant coral depletion throughout the Indo-Pacific. On the Great Barrier Reef, for example, CoTS outbreaks account for 42% of recorded coral loss from 1985-2012. Despite their importance, the demography and biology of CoTS is poorly understood, especially in terms of understanding the potential causes(s) of population outbreaks. For effective management of outbreaks, it is critical to understand the factors that both promote sudden population explosions, and that normally regulate CoTS populations at very low densities.

Predatory release has long been considered a potential contributor to population outbreaks of CoTS, initiating extensive searches for potential predators that may consume large numbers of these starfish at high rates, but are also vulnerable to over-fishing. As such, most research into predation on CoTS has focused on large reef fishes and invertebrates capable of capturing and consuming adult starfish. By contrast, consideration of smaller-bodied and potentially cryptic predators that could consume gametes, larvae or newly settled juveniles has received little attention. Thus, the overarching objective of this research was to explore predation on the early life stages of CoTS by two suites of predators: planktivorous damselfishes, and benthic invertebrates. Specifically, this research compares the predatory responses of a range of damselfishes, testing for interspecific variation in their potential importance as predators of CoTS eggs and larvae, and tests the influence of benthic predators on microhabitat preferences and settlement success of CoTS.

Although CoTS are equipped with anti-predator chemicals at every stage of their life cycle, the effectiveness of these chemicals in deterring predators is increasingly being questioned. In particular, planktivorous damselfishes, which are highly efficient zooplankton predators, may be capable of consuming the early life stages of CoTS in vast quantities, potentially reducing the reproductive and settlement success of this starfish. Nine planktivorous damselfishes are shown to readily consume food pellets that contain concentrations of up to 80% CoTS eggs, however all fishes exhibit increasing rejection of food pellets that contain higher proportions of eggs. This suggests that chemicals within the eggs are unpalatable, however palatability thresholds varied greatly among the damselfishes, indicating species that are likely to be more important as predators of CoTS eggs (or larvae). Notably, Amblyglyphidodon curacao consumed food pellets comprising 100% starfish eggs 1.5 times more than any other fish species, and appeared largely insensitive to increases in the concentration of starfish eggs. However, after standardising for size, smaller species, such as Pomacentrus moluccensis and Chrysiptera rollandi, consume a disproportionate amount of pellets comprising high proportions of starfish eggs and could be particularly important in regulating larval abundance and settlement success of CoTS.

To further explore the role of damselfish predation in potentially structuring CoTS populations, the feeding behaviour and functional responses of eleven damselfishes were examined by offering individual damselfish with increasing concentrations of larvae of either CoTS or Linckia laevigata (a co-occurring species with morphologically similar larvae). Consumption rates of CoTS larvae by damselfishes were independent of predator size, however when pooling across all predator species there was a significant negative relationship between predator size and consumption rate of L. laevigata. Most predatory species (all except A. curacao and Pomacentrus amboinensis) exhibited a Type II functional response, whereby the increasing feeding rate decelerated with increasing prey density. In addition, Acanthochromis polyacanthus and A. curacao, consumed larval CoTS at a greater rate than for L. laevigata, and consumption capacity of CoTS by Dascyllus aruanus was extremely high (158 larvae h⁻¹). These data reveal that a wide range of planktivorous fishes will prey upon CoTS larvae (at least when offered as the only available prey), and suggest that planktivorous damselfishes may have the capacity to buffer against population fluctuations of CoTS.

Predation rates on specific prey species can vary depending on availability of alternative prey. In the extreme, predators may exhibit prey switching, whereby they preferentially feed on the most abundant, or most readily accessible, prey species. Defining predatory responses to changes in prey availability is critical to evaluating the ability of predators to regulate prey populations. To extend the single-prey experiments, exploring prey preference and testing for prey switching, nine damselfishes were simultaneously offered varying relative densities of CoTS and L. laevigata larvae. Again, feeding responses varied among the damselfishes. While no evidence of prey switching was detected, five damselfishes (A. polyacanthus, A. curacao, Dascyllus reticulatus, P. amboinensis and P. moluccensis) exhibited increased consumption of CoTS larvae with increasing prey density, despite the availability of alternative prey. Moreover, Abudefduf sexfasciatus and P. amboinensis exhibited preference for CoTS larvae over L. laevigata larvae. These findings suggest that planktivorous damselfishes will consume CoTS larvae even in the presence of alternative, and presumably more palatable, prey. Further, most of the damselfishes responded to increasing larval CoTS densities by increasing theirprey intake, suggesting that they could be important in regulating successful settlement and recruitment, especially at low (non-outbreak) densities.

CoTS are also expected to suffer high levels of predator-induced mortality during settlement, as they transition to living in the benthic habitat and are exposed to an entirely new suite of predators. Accordingly, these larvae might be expected to exhibit behavioural adaptations, which serve to reduce predation at this critical stage in their life history. Pairwise choice experiments revealed that late stage brachiolaria larvae are able to detect predators in the substrate and where possible, will preferentially settle in microhabitats without predators. Settlement assays (without choices) revealed that larvae do not necessarily delay settlement in the presence of predators, but high levels of predation on settling larvae by benthic predators significantly reduce the number of larvae that settle successfully. Taken together, these results show that CoTS are highly vulnerable to benthic predators during settlement, and that variation in the abundance of benthic predators may significantly influence patterns of settlement and recruitment.

This research shows that eggs, larvae and newly settled CoTS are readily consumed by a wide range of coral reef organisms, such that predation during and soon after settlement may represent a significant bottleneck in their life history. Unfortunately, many of the predators that consume these early life stages are vulnerable to reef degradation and coral loss. Thus it is possible that anthropogenic degradation of reef ecosystems is contributing to the incidence and/or severity of CoTS outbreaks by mediating the abundance of these potentially key predators. Although it seems unlikely that predatory release in and of itself could account for initial onset of CoTS outbreaks, reducing anthropogenic stressors that reduce the abundance and/or diversity of potential predatory species represents a "no regrets" management strategy, but will need to be used in conjunction with other management strategies to prevent, or reduce the occurrence, of CoTS outbreaks.

Item ID: 51582
Item Type: Thesis (PhD)
Keywords: Acanthaster, Acanthasteridae, Bayesian analysis, behaviour, chemical defences, coral reefs, CoTS, crown of thorns starfish, damselfishes, data integration, fisheries closures, functional response, larvae, marine parks, mark-recapture, monitoring, population regulation, predation, predator removal hypothesis, resilience, saponins, top-down control, trophic cascades
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Cowan, Zara-Louise, Pratchett, Morgan, Messmer, Vanessa, and Ling, Scott (2017) Known predators of crown-of-thorns starfish (Acanthaster spp.) and their role in mitigating, if not preventing, population outbreaks. Diversity, 9 (1). pp. 1-19.

Chapter 3: Cowan, Zara-Louise, Ling, Scott D., Dworjanyn, Symon A., Caballes, Ciemon F., and Pratchett, Morgan S. (2017) Interspecific variation in potential importance of planktivorous damselfishes as predators of Acanthaster sp. eggs. Coral Reefs, 36 (2). pp. 653-661.

Chapter 4: Cowan, Zara-Louise, Dworjanyn, Symon A., Caballes, Ciemon, and Pratchett, Morgan (2016) Predation on crown-of-thorns starfish larvae by damselfishes. Coral Reefs, 35 (4). pp. 1253-1262.

Chapter 6: Cowan, Zara-Louise, Dworjanyn, Symon A., Caballes, Ciemon F., and Pratchett, Morgan (2016) Benthic predators influence microhabitat preferences and settlement success of crown-of-thorns starfish (Acanthaster cf. solaris). Diversity, 8 (4). pp. 1-11.

Appendix 1: MacNeil, M. Aaron, Mellin, Camille, Pratchett, Morgan S., Hoey, Jessica, Anthony, Kenneth R.N., Cheal, Alistair J., Miller, Ian, Sweatman, Hugh, Cowan, Zara L., Taylor, Sascha, Moon, Steven, and Fonnesbeck, Chris J. (2016) Joint estimation of crown of thorns (Acanthaster planci) densities on the Great Barrier Reef. PeerJ, 4. pp. 1-17.

Date Deposited: 20 Nov 2017 01:14
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 80%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060808 Invertebrate Biology @ 20%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 80%
96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960402 Control of Animal Pests, Diseases and Exotic Species in Coastal and Estuarine Environments @ 20%
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