diversity Review Known Predators of Crown-of-Thorns Starfish (Acanthaster spp.) and Their Role in Mitigating, If Not Preventing, Population Outbreaks Zara-Louise Cowan 1,*, Morgan Pratchett 1, Vanessa Messmer 1 and Scott Ling 2 1 ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia; [email protected] (M.P.); [email protected] (V.M.) 2 Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS 7001, Australia; [email protected] * Correspondence: [email protected]; Tel.: +61-7-4781-5747 Academic Editors: Sven Uthicke and Michael Wink Received: 20 November 2016; Accepted: 17 January 2017; Published: 22 January 2017 Abstract: Predatory release has long been considered a potential contributor to population outbreaks of crown-of-thorns starfish (CoTS; Acanthaster spp.). This has initiated extensive searches for potentially important predators that can consume large numbers of CoTS at high rates, which are also vulnerable to over-fishing or reef degradation. Herein, we review reported predators of CoTS and assess the potential for these organisms to exert significant mortality, and thereby prevent and/or moderate CoTS outbreaks. In all, 80 species of coral reef organisms (including fishes, and motile and sessile invertebrates) are reported to predate on CoTS gametes (three species), larvae (17 species), juveniles (15 species), adults (18 species) and/or opportunistically feed on injured (10 species) or moribund (42 species) individuals within reef habitats. It is clear however, that predation on early life-history stages has been understudied, and there are likely to be many more species of reef fishes and/or sessile invertebrates that readily consume CoTS gametes and/or larvae. Given the number and diversity of coral reef species that consume Acanthaster spp., most of which (e.g., Arothron pufferfishes) are not explicitly targeted by reef-based fisheries, links between overfishing and CoTS outbreaks remain equivocal. There is also no single species that appears to have a disproportionate role in regulating CoTS populations. Rather, the collective consumption of CoTS by multiple different species and at different life-history stages is likely to suppress the local abundance of CoTS, and thereby mediate the severity of outbreaks. It is possible therefore, that general degradation of reef ecosystems and corresponding declines in biodiversity and productivity, may contribute to increasing incidence or severity of outbreaks of Acanthaster spp. However, it seems unlikely that predatory release in and of itself could account for initial onset of CoTS outbreaks. In conclusion, 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. Keywords: Acanthaster (Acanthasteridae); fisheries closures; marine parks; predation; predator removal hypothesis; chemical defences; saponins; population regulation; top-down control; trophic cascades 1. Introduction Adult crown-of-thorns starfish (CoTS; Acanthaster sp.) have numerous long, very sharp and toxic spines (Figure1). In addition, the dermal tissues of CoTS (and all of their organs) contain high concentrations of chemicals, including saponins [1,2] and plancitoxins [3], which are both Diversity 2017, 9, 7; doi:10.3390/d9010007 www.mdpi.com/journal/diversity Diversity 2017, 9, 7 2 of 19 unpalatable [4] and highly toxic [5–7]. Intuitively therefore, one might expect that these starfish are effectivelyDiversity 2017, protected9, 7 and largely immune from predation (e.g., [8]). In reality, there2 of are 19 few organisms that are completely immune to predation at any or all stages of their life cycle. Rather, well-developedunpalatable [4] anti-predatory and highly toxic defences [5–7]. Intuitively reduce thetherefore, range one of predatorsmight expect to that which these prey starfish species are are effectively protected and largely immune from predation (e.g., [8]). In reality, there are few vulnerable [9], but may or may not affect overall rates of predation and the extent to which prey organisms that are completely immune to predation at any or all stages of their life cycle. Rather, populationswell-developed are controlled anti-predatory by predators. defences Accordingly,reduce the range there of predators is an increasing to which number prey species of coral are reef organismsvulnerable (fishes [9], andbut invertebrates)may or may not reported affect overall to predate rates of on predation CoTS [10 and,11 ],the including extent to somewhich predatorsprey (e.g.,populationsArothron pufferfishes) are controlled that by feedpredators. almost Accordingly, exclusively there on adultis an increasing CoTS when number they areof coral in abundant reef supplyorganisms (e.g., during (fishes outbreaks). and invertebrates) Such predators reported mayto predate be important on CoTS in[10,11], supressing including the some abundance predators of prey species(e.g., [12 Arothron] as well pufferfishes) as influencing that feed the behaviour,almost exclusively habitat-associations, on adult CoTS when and populationthey are in abundant dynamics of evensupply well-armoured (e.g., during and/or outbreaks). chemically Such predators defended may prey be species important (e.g., in [supressing13]). the abundance of Despiteprey species their [12] physical as well and as chemical influencing defences, the behaviour, post-settlement habitat-associ stagesations, (juvenile and population and adults) of CoTSdynamics often exhibit of even injuries, well-armoured largely manifestedand/or chem asically missing defended arms prey [11 species,14,15]. (e.g., These [13]). injuries are believed Despite their physical and chemical defences, post-settlement stages (juvenile and adults) of to occur when predators are only able to remove one or a few arms before the starfish escapes or CoTS often exhibit injuries, largely manifested as missing arms [11,14,15]. These injuries are believed avoidsto occur further when damage predators by hidingare only within able to theremove reef one matrix or a [few15]. arms If however, before the there starfish are escapes highrates or of partialavoids predation further at damage specific by reef hiding locations within [11 the] then reef it matrix is expected [15]. If at however, least some there CoTS are willhigh alsorates be of killed outrightpartial and/or predation consumed at specific in entirety. reef locations The cryptic [11] then nature it is andexpected nocturnal at least behaviour some CoTS of CoTS,will also especially be whenkilled small outright (<12 cm and/or diameter) consumed or at in low entirety. densities The cryptic [11,16 ]nature further and suggests nocturnal that behaviour they must of CoTS, be highly vulnerableespecially to predators. when small In (<12 controlled cm diameter) experiments, or at low survivorshipdensities [11,16] of further laboratory suggests reared thatAcanthaster they must spp. settledbe tohighly natural vulnerable substrates to predators. is effectively In controlled zero, owing experiments, to very highsurvivorship rates of of predation laboratory by reared naturally occurringAcanthaster predators spp. settled [17–19 to]. Recentnatural researchsubstrates also is effectively demonstrates zero, owing that CoTS to very larvae high arerates highly of predation vulnerable to predationby naturally [20], occurring despite having predators the highest[17–19]. concentrationsRecent research ofalso anti-predator demonstrates chemicals that CoTS (discussed larvae are later). highly vulnerable to predation [20], despite having the highest concentrations of anti-predator Cowan et al. [20] showed that CoTS larvae are readily consumed by many common planktivorous chemicals (discussed later). Cowan et al. [20] showed that CoTS larvae are readily consumed by damselfishes,many common and often planktivorous in preference damsel tofishes, other and asteroid often in larvae. preference to other asteroid larvae. WhileWhile there there is nowis now general general acceptance acceptance thatthat CoTS are are vulnerable vulnerable to topredation predation (e.g., (e.g., [11,21]), [11 ,21]), on-goingon-going controversies controversies relate relate to whetherto whether known known predators predators would would ever ever be be capable capable of of regulating regulating CoTS populations,CoTS populations, and mitigating, and mitigating, if not preventing if not preventi outbreaks.ng outbreaks. More specifically, More specifically, attention attention is focussed is on whetherfocussed anthropogenic on whether impactsanthropogenic (viafishing impacts or (via habitat fishing degradation) or habitat degradation) have supressed have supressed the abundance the of keyabundance predators, of thereby key predators, accounting thereby for the accounting seemingly for recent the seemingly and/or increasing recent and/or occurrence increasing of CoTS outbreaksoccurrence [10]. of CoTS outbreaks [10]. FigureFigure 1. Adult 1. Adult crown-of-thorns crown-of-thorns starfish starfish are are defended defended against against predators predators by by numerous numerous long, long, very very sharp and toxicsharp spines. and toxic Photographic spines. Photographic credit: Scott credit: Ling, Scott Dick’s Ling, Dick’s Reef, SwainsReef, Swains Region, Region, southern southern Great Great