The Giant Triton (Charonia tritonis) may effect aggregation and fertilisation success of the Crown of Thorns Starfish (Acanthaster planci)
1. General Background
Outbreaks of the crown of thorns starfish (Acanthaster planci) have been studied for many years throughout the Indo-West Pacific region (Moran, 1986) and although many explanatory hypotheses have been proposed we do not understand why outbreaks of this starfish occur on some reefs while, on other nearby reefs, this starfish maintains a stable, low population density. On the Great Barrier Reef and elsewhere, most starfish research has centred on establishing the scale of Acanthaster outbreaks and the effect of Acanthaster predation on the coral reef community. The giant triton (Charonia tritonis) and other members of the genus Charonia are known predators of many species of starfish (Chesher, 1969; Endean, 1969; Laxton, 1971; Noguchi et al., 1982; Percharde, 1972) but there are few examples of other species predominantly preying on starfish (Harrold and Pearse, 1987) with the possible exception of other starfish (Birkeland et al, 1982; Dayton et al, 1977; Mauzey et al, 1968). Endean (1969) proposed that predation on starfish plays an important role in starfish population stability and discussed the possible causes of Acanthaster outbreaks with particular emphasis on the removal by humans of the predators of adult and juvenile starfish. While it is recognised that predation can determine the spatial patterns of natural communities (Paine, 1966; Janzen, 1970; Connell, 1971) and can represent powerful selective pressure in the evolution of prey adaptation (Schmitt, 1982), the role of natural predators in maintaining high prey diversity, and the possible survival strategy of rarity in the coral reef community is unclear with respect to either starfish, their predators or their prey.
A high to low latitudinal increase in gastropod anti-predatory structures was found by Vermeij (1978) and Blake (1983) suggested the existence of a similar pattern in sea stars. Cameron and Endean (1982) discussed the role of venomous devices and toxins as defences against predation and Blake commented that the asteroid fauna of the Indo-West Pacific are dominated by the order Valvatida and members of this order have the best developed anti-predatory devices. Yamaguchi (1975) commented on the difference between adult and juvenile asteroid habits and suggested that the heavy armour of exposed adult asteroids might reflect “heavy predation pressure, presumably by fish” (emphasis added). Other structures that provide protection from predation include the venomous spines of Acanthaster (Blake, 1983; Endean, 1969), and the pedicellaria which are highly diverse, that distinguish the phylum Echinodermata. In addition to structural protection, many species of starfish reduce predation by the possession of skin toxins (Riccio et al., 1982, 1985; Gorshkov et al., 1982; Minale et al., 1984) and these have been shown to be toxic to some fish species (Rideout, 1975). Riccio et al. examined the steroidal glycosides present in the starfish Linckia laevigata and Echinaster luzonicus and Gorshkov et al studied the effect of marine glycosides on ATPase activity. The role of echinoderm toxins as a defence against predation has been discussed extensively (Bakus, 1974; Green, 1977). It has been proposed that the production of toxins for defence incurs an energy cost which is balanced against the probability of mortality (Eckardt, 1974) but in some species, toxins might be metabolic by-products that incur no energy cost in their synthesis. The results of Noguchi et al. (1982) where tetrodotoxin from the starfish Astropecten polyacanthus caused the toxification of Charonia sauliae and the fact that toxic starfish species are regularly preyed upon by Charonia tritonis (Endean, 1968; Chesher, 1969; Percharde, 1972) demonstrates that this gastropod genus is unaffected by the toxins present in many species of starfish. In some groups of starfish behavioural mechanisms are used as defences against predation and within the order Paxillosida two important tropical exceptions from the generally armoured rule, that of Astropecten and Luidia, were distinguished and discussed by Blake (1983). It was suggested that both genera had broad open ambulacral furrows because they were predators on active solitary forms where increased skeletal mobility was essential. Because both these active, hunting genera live on and within unconsolidated sediment they avoid predation by burrowing and this is facilitated by the paxillose nature of their aboral surface. Another behavioural defence in asteroids is the autotomy of arms and some species can regenerate complete starfish from a section of one arm. Cameron and Endean (1982) suggested that autotomy is an adaptation to predation and Aldrich (1976) noted for Asterias forbesi that autotomy occurred readily in response to attack by a decapod crustacean. Birkeland et al (1982) obtained similar results in their study of asteroid predatory interactions. A number of tropical and temperate asteroids are known to undergo regular autotomy (Rideout, 1978; Yamaguchi, 1975) and Blake (1983) commented that interpretation of the skeleton can be difficult as it has more than one function and protection against predation can be accomplished by many mechanisms.
High population densities of starfish have been observed in many studies of temperate communities and some starfish species are of economic significance as predators of commercial shellfish. In temperate studies of starfish it is usual to regard the starfish as the predator and a mollusc as the prey, with the molluscan escape response being well documented (Kohn, 1961; Schmitt, 1982), and amongst motile benthic invertebrates, the classic defence against predation (Feder, 1963; Ansell, 1969; Phillips, 1976). Bullock (1953) found that gastropods were located in the same area but usually not close to predatory sea stars and Kohn (1961) suggested that escape responses have a role in determining distribution patterns in nature. The cannibalistic starfish Meyenaster gelatinosus demonstrates a well developed escape response when contact is made with conspecifics (Dayton et al, 1977) and this response includes the autotomisation of arms. Jost (1979) suggested that predator avoidance could account for an observed negative correlation between one species of starfish and its prey while another starfish species showed a positive correlation with the same prey species. In two species of subtidal gastropod, the role of this defence was closely examined by Schmitt (1982) who found that the presence of predatory starfish could trigger the migration of their prey and Schmitt concluded that prey defence can play a central role in determining patterns of prey distribution and abundance.
Chesher (1969) noted that Charonia tritonis can detect and actively seek out its prey and when contact is made Acanthaster planci recognises the predator and moved away rapidly. Paterson and Poulsen (1986) demonstrated a strong avoidance reaction by Acanthaster when one of its sensory tentacles makes physical contact with the body of Charonia. Percharde (1972) described the attack of the Caribbean triton (Charonia tritonis variegata) upon a breeding aggregation of the starfish Echinaster sentus and concluded that this mollusc plays an important role in the ecological balance of extensive areas of its habitat. Laxton (1971) stated that the New Zealand species of Charonia preys upon the most common large echinoderm in the area but if a choice is offered, Charonia from all habitats prefer the cushion star Patiriella regularis followed closely by Coscinasterias calamaria. While Charonia has been collected by humans for our entire recorded history, it is difficult to determine the extent to which its abundance has been reduced by human activities but it has generally been regarded as not common on the Great Barrier Reef. On the Great Barrier Reef the preferred prey of Charonia tritonis appears to vary and Endean (1969) stated that it was an unspecified species of Nardoa. Recent observations of Charonia behaviour (Paterson and Poulsen, 1986-1989) demonstrated a well developed escape response by Acanthaster planci to the presence of Charonia tritonis and suggested that the correct prey preference of Charonia on the Great Barrier Reef may be Acanthaster. These results confirmed the observations of Endean that on outbreaking reefs, Acanthaster planci is the predominant prey of Charonia tritonis. Aquarium studies also confirmed that Acanthaster can be actively hunted by Charonia to the point of local extinction despite the presence of other, less mobile starfish genera, including Nardoa and Linckia. The high mobility of species such as Acanthaster planci and Coscinasterias calamaria may result in large specimens of these species escaping complete predation and their survival following predator attack may result in confusion between prey preference and prey capture. If this is true it will require a reappraisal of the results of Endean (1969) and Laxton (1971) with respect to the prey preference of Charonia. It is necessary to distinguish clearly between starfish species that attract Charonia and which it prefers to consume and alternately starfish species that are sufficiently slow moving that Charonia capture and consume them regularly. It is suggested that this distinction is relevant to the mechanism that regulates Acanthaster and Coscinasterias numbers when their populations are at low density. The ability of Charonia to regulate low population numbers of Acanthaster is dependent on its ability to locate and attack aggregations of Acanthaster even when this starfish is less common than other genera such as Linckia and Nardoa. This would also be true with respect to predation of Coscinasterias and Patiriella. The effectiveness of predation or dispersal as a means of starfish population regulation will be less dependent on the feeding rate and more dependent on the prey preference of Charonia when the starfish are at low population density.
Paterson and Poulsen, 1986-1989 suggested that Charonia tritonis may aggregate in regions of an outbreaking reef that contain the greatest Acanthaster planci abundance during the post-outbreak phase. It was suggested that such aggregation could result from either a direct attraction of the predator to its prey or alternately increased predator activity when food is scarce. The activity of the predatory starfish Astropecten aranciacus is known to depend on prey density (Ribi and Jost, 1978). Because Charonia tritonis is predominantly cryptic, it is extremely likely that a cursory examination of a reef will greatly underestimate its abundance and before an accurate estimate of the abundance of Charonia can be made on either a non-outbreaking reef such as Heron Reef or an outbreaking reef such as John Brewer Reef, it is necessary to establish whether Charonia aggregates. If aggregations occur in the vicinity of Acanthaster or other starfish aggregations then density estimates of Charonia must be stratified with respect to this variable because it is relevant to an expected non-random distribution of Charonia numbers. While a large-scaled negative correlation between Acanthaster and Charonia abundance is predicted by the Predator Control Hypothesis (Endean, 1969), a medium-scale positive correlation will be predicted if Charonia aggregate in areas of Acanthaster aggregation. The observation of Acanthaster escape following Charonia attack would imply a further negative correlation between Acanthaster and Charonia on an even finer scale. The low abundance of all large-bodied species of starfish on Heron Reef (Paterson, 1996) and other non-outbreaking reefs (Paterson, 1990) is in contrast to data from outbreaking reefs (Paterson and Poulsen, 1986-89), and supports the suggestion of Laxton (1974) that on outbreaking reefs, the abundance of other species of starfish decline during the period between outbreaks of Acanthaster planci. At John Brewer Reef between 1986 and 1988, the prey preference and aggregated spatial pattern of Charonia tritonis seemed sufficient to account for the observed reduction in Acanthaster planci numbers within the relatively small area of residual starfish outbreak. It is possible that a similar sized but dispersed population of Charonia at Heron Reef could remain undetected but be sufficient to explain the low abundance of all starfish species on that reef. It was suggested by Paterson (1990) that high general starfish abundance at the end of the recovery phase of an outbreaking reef may indicate primary outbreak preconditions and be related to low Charonia abundance.
Ormond et al. (1973) discussed the consequences of spawning aggregations of Acanthaster and suggested that the increased proximity of adult starfish may enhance the chances of fertilisation, especially if synchronous spawning takes place. Further, they suggested that the population density of Acanthaster at which aggregation into groups begins may constitute a threshold beyond which a population explosion (outbreak) is likely to occur. Populations of all species of starfish will be sensitive to changes which result in densities in the region of this threshold. It was suggested by Beach (1975) and Lucas (1984) that a conspecific stimulus would induce synchronous spawning in Acanthaster planci and a delayed spawning activity in dispersed individuals of Acanthaster planci was observed by Okaji (1991). It was suggested that this delay reflected less frequent stimulus from conspecifics in dispersed compared with aggregated populations and that synchronous spawning induced by such stimulus would lead to higher rates of fertilisation when the animals formed an aggregation. The effect of sperm dilution, adult aggregation and synchronous spawning upon the fertilisation of sea-urchin eggs was reported by Pennington (1985). Pennington concluded that significant fertilisation occurred only when spawning individuals are closer than a few metres. The consequences of water mixing and sperm dilution for species that undergo external fertilisation were discussed by Denny and Shibata (1989) who found that only a small fraction of ova were fertilised other than in densely packed arrays. They commented that the low effectiveness of external fertilisation may change the way one views the planktonic portion of such life cycles and suggested that this could serve as a potent selective factor. For the rarer sexually reproducing species it is apparent that the occurrence of an opposite sexed conspecific within the effective fertilisation distance is a condition precedent to successful reproduction and the degree of success may be strongly dependent on just how close the rare spawning individuals are to each other. This is considered to be of fundamental importance to starfish egg fertilisation because the degree of egg fertilisation would not be expected to be an inverse linear relationship with distance between opposite sexed spawning individuals under turbulent water conditions when individuals are widely spaced (Denny and Shibata, 1989). Under conditions of perfect water mixing, the probability of an egg’s fertilisation will be inversely proportional to the square of the distance between individuals in shallow water (approximately two dimensional sperm dilution) and inversely proportional to the cube of this distance in deep-mid water (three dimensional sperm dilution). Clearly, the natural spawning environment of Acanthaster is somewhere between these two extremes.
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