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Crown-of-thorns starfish on the great barrier reef
Crown-of-thorns starfish on the Great Barrier Reef Robert Endean During the 1960s and 1970s the bulk of the hard coral cover of reefs in the central region of Australia’s Great Barrier Reef was killed as a result of population outbreaks of the coral-eating starfish, Acanthaster plunci. Millions of starfish were involved. Renewed outbreaks have recently been noted on reefs where extensive recolonization has occurred since the mid-1960s, giving rise to concern that reefs in the region will be impoverished for long periods of time. The causes of the population outbreahs are unknown, but there is evidence of human involvement in triggering the population outbreaks. Green Island is a coral cay situated on an extensive platform reef lying off the eastern Queensland coast near the city of Cairns. Named in 1770by Captain James Cook after William Green, one of the scientists carried on board the Endeavour (1768-71) during its epic voyage of discovery along the eastern Australian coast, the island was first settled in the 1870s by collectors of b&he-de-mer. Since that time the reef at Green Island has been visited regularly, first by b&he-de-mer and trochus gatherers, then by fishermen, reef fossickers, tourists, and divers. It has been a tourist resort for decades and its underwater observatory and glassbottomed boats for coral viewing are stated to have been among the first to operate in the world. Prior to 1962, it had been widely acclaimed in magazine articles, books, and tourist brochures as a reef that carried luxuriant coral. Then disaster struck. In 1962coral colonies on the Green Island reef were observed to be attacked and killed by very large numbers of Acanthaster planci, a coral-eating starfish known as the crown-of-thorns starfish [l]. The progress of the A. planci infestation at Green Island reef in the early 1960swas described by J. H. Barnes [2]. Despite attempts to collect and remove A. planci from areas of the reef most frequently visited by tourists, the bulk (about 80 per cent) of the hard coral cover of the reef had been destroyed by the end of 1966 [3] [4]. Prior to 1962no accounts of similar destruction of the hard coral cover of reefs by A. plunci had been reported in the scientific literature. However, it has since been reported that the reef at Miyako Island in the Ryukyus south of Japan was infested with A. planci in 1957. In that year more than 220,000 specimens were collected during a government-sponsored control programme [5]. This appears to be the first outbreak of A. planci ever recorded. Apparently there are no historical records of population outbreaks of A. planci in the Robert Endean, M.Sc., Ph.D Was born in New South Wales, Australia, and is a graduate of the University of Sydney. Trained as a marine biologist, he developed interests in the ecology of coral reef communities and in the toxins produced by marine animals. Since 1950 he has been on the staff of the Zoology Department, University of Queensland, and is currently Reader in Zoology. Endaevour, New Sarie+ Volume 6, No. 1 1982 (0 Pergamon Press, Prmted in Great Britainl. OlSCL9327/82/03110/05/$003.00
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Indo-West Pacific region. Indeed, in the Ryukyus A. planci is called ‘America-yui’ because outbreaks were observed there for the first time during the American occupation following World War II [6]. By 1967the numbers of A. plunci on the reef at Green Island had obviously begun to decline and few could be found there in 1968. During the period of infestation the reef community had changed from one dominated by corals to one dominated by algae. There had also been a concomitant change in the fauna formerly associated with living corals leading to an obvious reduction in species diversity. Within 14-21 days after the skeletons of coral were exposed as a result of the feeding activities of A. planci, filamentous algae began to grow on the white exposed skeletons, which soon acquired a dark coating of algae. For months, the devastated reef presented a drab picture relieved only by the occasional live massive coral or patch of live branching coral bypassed by the voracious starfish. Gradually the picture changed. Coralline algae and stalked algae aswell assoft corals proliferated in many shallow-water areas. Three to four years after destruction of an area of hard coral small colonies of recolonizing hard corals were evident. Well-known opportunistic species such as Pocillopora damicornis, Seriatopora hystrix, and Stylophora pistillatu were among the first to settle. Fast-growing tabular colonies of Acropora hyacinthus then became well represented and these appeared to dominate subsequent stagesof recovery. By 1979, some 17 years after obvious damage to the hard coral cover of the reef was first observed, a good coral cover had been re-established at Green Island reef. However, it is unlikely that the climax stage in the recolonization process had been reached. In December, 1979, acting on information supplied by fishermen that Green Island reef was again under attack by A. planci, a party from the University of Queensland, led by the author: paid it a visit. Large numbers of adult and juvenile A. planci were seen (figure 1) and these were obviously causing extensive damage to the hard coral cover of the reef. Transects were run at several locations on the reef and, by using techniques applied in earlier surveys [7] [8], it was estimated that approximately 60 per cent of the hard coral cover of the reef had been recently killed by A.planci. The adult starfish population of the reef was estimated to be about
Figure 1 Specimens of crown-of-thorns starfish eating coral c thegenusAcroporaonthereefflat,GreenIsland.Januaryl981. Parts of the white skeletons of the coral are exposed.
Port
Douglas CAIRNS
*.Broadhurst
)i:k’.e
Reef
Reef :Tideway .._ .,
QUEENSLAND
Figure 2 Typical appearance of algae-covered skeletons coralsofthegenusAcroporakilledbythecrown-of-thorns starfish on the reef flat, Green Island, January 1981.
of plz rte
Reef
‘,BunkerGroup \
Figure3 Acrown-of-thorns starfish feeding on a massive hemisphericalcoralofthegenusPoritesonthereefflat,Green Island, Jannary, 1981.
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Figure4 MapofportionoftheQueenslandcoastshowingthe Great Barrier Reef region and localities mentioned
in the text.
Figure 5 Aggregations of crown-of-thorns starfish feeding on platecoraIsofthegenusAcroporaatHowieReef,Januan/,1981
11
350,000. This was possibly an underestimate, since soon afterwards the Australian Minister for Science was quoted in local newspapers as stating that government scientists estimated that approximately two million A. planci were present on Green Island reef. In January 1981 we resurveyed the reef and it was estimated that approximately 90 per cent of the hard coral cover of the reef had been killed (figure 2), and destruction of the remainder was in progress. Even large massive corals that, judging by their size, had been bypassed during the A. planci infestation in the 1960s were under attack (figure 3). Since our previous visit signs had been erected on the cay at Green Island by the Queensland government warning tourists of the danger of treading on the venomous spines of the starfish. The reefs of the Great Barrier Reef affected by the outbreaks Although population outbreaks of A. planci were
use by clam poachers who, prior to 1980, ravaged the reefs in the area. Be this as it may, reefs near these cays appear to have been among those most frequently visited by humans in the Swain Reefs complex. Most visitors taken, to the area by charter-boat operators engage in activities-such as line fishing, spear fishing, and shell collecting-that involve collecting elements of the fauna. Study of all reefs affected by the A. planci population outbreaks during the period 1962-1974 indicates the likelihood1 that1the [reefs, first affected,in each area were the ones most visited by humans. In 1975 reefs near lat. 14”s were found to be infested and in 1980 and 1981 the author and associates established that several reefs lying between lat. 16” 30’S and lat. 17” 30’S which had been infested with A. planci in the 1960s were again carrying population outbreaks of A. planci (figure 5). Biology of Acanthasterplanci
observed on several reefs near Green Island in 1962, it is A. planci is a large (up to 60 cm diameter) multi-armed not known whether the outbreaks began on all of them starfish. Its upper surface is covered with stout spines simultaneously. No outbreaks were observed on any that have given rise to its common name, the crown-ofreefs of the Green Barrier Reef prior to the 1960s. thorns starfish. Toxic saponins occur in the skin overHowever, in the period 1962 to 1974 inclusive the lying the spines and A. planci is the only venomous majority of the approximately 300 platform reefs of the starfish known. When adult, it appears to prey principally on acroporid corals and is apparently confined to coral Great Barrier Reef lying between lat. 14” 40’S and lat. 20% (figure 4) experienced such outbreaks [9]. In most reefs. It has the ability to utilize cetyl palmitate, the cases the bulk of the hard coral cover of those reefs major wax energy reserve of corals. In the past it has been regarded as a rare animal but its normal population examined was destroyed within two to four years [lo]. Tens of thousands of starfish are believed to have been density on reefs of the Great Barrier Reef was not present on a reef during an infestation. Subsequently A. known until 1972. In that year the services of about a planci disappeared from each reef, and as no mass hundred trained divers were utilized to determine mortality was observed at any stage it is assumedthat the population densities of A. planci on several uninfested starfish migrated from the devastated reefs. In a few reefs of the Great Barrier Reef that carried an apparentinstances invasion of a reef by adult A. planci arriving at ly normal coral cover. A figure of approximately 6 specimens (all mature adults) per km* was obtained [lo]. the base of the seaward slopes of a reef, presumably after migrating there from an adjacent reef, was witnes- This figure agreed well with earlier estimates for reefs in the central pacific region [ll] and for reefs in the Red sed. Occasionally only juvenile starfish were present in large numbers on a reef, but in many casesinfested reefs Sea [12]. Thus the starfish can be considered a rare, as well as a highly specialized carnivore found on coral carried both adults and juveniles. During the period 1962-1974 the principal direction of the spread of the reefs. It has been calculated that a mean density of about 14 infestations was from reefs near Cairns to others progressively further to the south [9], but this is not to imply adult specimens of the starfish per 1000m* is sufficient to kill the bulk of the hard coral cover of a reef of average that there was a front of invading starfish moving relentlessly southwards. In retrospect, it now seems size (10 km* in flat projection) in 2.5 years, during which time recolonization by hard corals is negligible. This likely that certain platform reefs, first in the region lying between the latitudes of Port Douglas and Innisfail and represents an increase by a factor of about 2,330 in the subsequently in areas further to the south and to the normal population density of A. planci on uninfested reefs. Obviously it is not resource-limited at normal north, became infested and acted as foci for the infestation of adjacent reefs, including outer platform reefs in population density. Other features of its life history that have relevance each area. Certainly reefs such as Rib Reef, Broadhurst for the present discussion are its great fecundity (each Reef, Line Reef, and Tideway Reef became infested female having the potential to release millions of eggs), before other reefs in their vicinity. A few reefs outside the region extending from lat. 14” its limited breeding season, and the presence in its life 40’S to lat. 20% became infested in the period 1962- cycle of planktotrophic larval stages of long duration. After settlement and metamorphosis juveniles eat cora1974. Some of them were lagoon reefs in the Bunker line and other epiphytic algae. They grow rapidly and at Group near the southern end of the Great Barrier Reef. an age of 4-5 months they resemble miniature adults and Others were located in the Swain Reefs complex [lo]. have adopted adult feeding behaviour. When one year The initial infestation in the Swain Reefs complex involved reefs near Lavers Cay (approximately lat. 21” old they are 6 to 7 cm in diameter. A diameter of 20 cm is 10’S) and Mystery Cay (approximately lat. 21” 20’S) reached by specimens aged between 1% to 2 years. Specimens become sexually mature when 14-16 cm in which are among the most remote reefs of the Great Barrier Reef. However, charter-boat operators use diameter. The age attained by large specimens of A. these cays as aids in navigating the labyrinthine maze of planci is not known, but is certainly in excess of five years. reefs in the area, and no doubt they were put to a similar 12
Mortality at different stages in the life history is not known. Predators of juvenile A. plunci on reefs in Great Barrier Reef waters include xanthid crabs and the groper, Promicrops lanceolatus. Known predators of, adult starfish on the Great Barrier Reef include the giant triton, Charonia tritonis and the large wrasse, Cheilinus undulatus. Although large adults frequently lose one or more arms to predators on reefs they appear to survive such attacks. It is possible that other reef fishes are also predators of juvenile and/or adult starfish. Certain puffer fishes and trigger fishes have been shown to be predators of adult A. planci in the Red Sea [12]. Possible causes of the outbreaks
Despite a considerable amount of research since a previous review [13] in this journal in 1971 of the A. plunci problem on the Great Barrier Reef, it is still not possible to state the cause or causes of the population outbreaks. The various hypotheses that have been proposed to account for the outbreaks fall into two groups. Those in one group might be termed the normal event hypotheses, and those in the other the abnormal event hypotheses. Many of those belonging to the first group can be readily refuted [14]. Others which relate to natural fluctuations in the breeding successof A. plunci [15][16] are more difficult to refute. Because the starfish has a high fecundity and planktotrophic larval stages, environmental conditions could be more conducive to the production and survival of large numbers of larvae in some years than in others. Infestations of reefs could occur in the years in which large numbers of larvae are recruited. However, the A. plunci population structures found on infested reefs of the Great Barrier Reef were usually polymodal, indicating the existence of several year classes[7]. Further, the infestations have continued since the early 1960s.All this renders it unlikely that the outbreaks could be the direct result of exceptional recruitment in one particular year or even in a number of successive years. Then, too, it has become apparent that, at any one time, some reefs in a particular area may suffer population outbreaks while others in the same area may not. This suggeststhat the infestations are not necessarily the result of abnormally large numbers of larvae being present in the plankton at a particular time. Rather does it suggestthat some reefs are more prone to infestation than others in the same area. None of the normal event hypotheses indicate why this should be so. There remain the hypotheses that the A. plunci population outbreaks are abnormal events. K. W. F. Watt [17] has written that ‘It should be noted that a great many of the species in the world are so rare that they have attracted little attention, and also may be quite stable in numbers which would also prevent them from attracting attention’. Prior to the middle of this century A. planci appears to have been such a rare species. There is an absence of scientific or historical records providing unequivocal evidence of A. planci infestations of reefs prior to the 1950s although the venomous nature of the species was well known to the indigenous peoples of the tropical West Pacific region. The discovery of Acanthaster debris in sediments on several reefs of the Great Barrier Reef [18] was claimed to be evidence of previous ‘plagues’ of the starfish on these reefs. However, information was not provided on how
many skeletal remains of A. planci per kg of sediment represent a past ‘plague’. The apparent absence of any mass mortality among starfish present on a reef during an infestation raises problems in interpreting the significance of the debris. Difficulties are also encountered in accounting for the retention of Acanthuster debris on platform reefs which reached the surface hundreds of years ago and which are growing on antecedent knolllike structures. As already noted, A. plunci has the attributes of a rare and specialized carnivore belonging to the coral reef community. These communities are regarded by many biologists as having a particularly stable or predictable organization because they possessnumerous homeostatic mechanisms which buffer any tendency for marked change in the population densities of constituent species. In the case of A. plunci only a modest increase in the normal population density of the species is required to obliterate the basic element of the coral reef community, the hard coral cover. Obviously, the number of starfish present must normally be regulated within narrow limits. The fact that population outbreaks have occurred suggests that a perturbation of a novel kind with which existing homeostatic mechanisms cannot cope, or which entirely disrupts these mechanisms, has been introduced into the system. What is this perturbation? The observation that infestations appear to have begun on the Great Barrier Reef and elsewhere [5] on accessible reefs visited by humans suggests human involvement in initiating them. It is difficult to perceive a mechanism whereby human activities could increase the success of recruitment of larval A. planci to a reef. Pollution, by selectively eliminating larval predators, comes to mind but should affect recruitment of A. planci to all reefs in any area rather than affecting one or a few reefs. Then again, pollution could hardly be involved in facilitating recruitment to remote reefs in the Swain Reefs complex. If attention be concentrated on the possibility that human activities might have an effect on part-larval starfish populations, then a mechanism for the population outbreaks suggestsitself. Since neither adult nor juvenile starfish are resource limited when present on reefs at normal population density, it seems likely that their populations are normally controlled by predators. Release of predator pressure on post-larval stages as a result of human activity could be a key factor in triggering the infestations. Because their size, venomousness, and ability to regenerate missing parts render large adult starfish less vulnerable to predators than juveniles and small adults, predation on juveniles and small adults could have greater significance than predation on large adults. The giant triton, Charonia tritonis, is an important predator on large juvenile and small adult A. planci, and gropers (Promicrops lanceolatus) are known to prey on juvenile A. planci. Evidence has been obtained of an extensive trade in giant tritons in Great Barrier Reef waters and many reefs there have been overfished, particularly by spear-fishermen [19] [20]. Excessive collecting by humans of giant tritons and resident reef fishes, especially groper, could well have been responsible for initiating the A. planci outbreaks. Such an hypothesis is in accord with the history of the population outbreaks, with their locations, and with the views of many biologists on the 13
organization of coral reef communities. Moreover, it should be possible to test the hypothesis in the field. Possible consequences
of the outbreaks
It is believed that the bulk of the hard coral cover of the majority of platform reefs in the central region of the Great Barrier Reef was devastated by A. planci population outbreaks during the 1960s and 1970s. The longterm ecological consequences of the destruction of this huge amount of coral are difficult to predict. Particularly is this so because population outbreaks are now reoccurring on these reefs as their hard coral cover is re-established. It seems likely that the factors which have triggered the original outbreaks are still operative. This could lead to impoverishment for decades of reefs in the central region of the Great Barrier Reef. Furthermore, infestations are now occurring on some reefs to both the north and south of the central region. This suggests that the perturbations responsible for the infestations are now operating outside the central region and opens up the possibility that the whole Great Barrier Reef ecosystem could ultimately be affected. As well ashaving serious ecological consequences, the A. planci population outbreaks could have serious economic consequences. Several workers who have studied the phenomenon have commented on the dearth of resident fishes on reefs affected by the population outbreaks. It is of interest to note that commercial fishing for reef-associated fishes has now virtually ceased on reefs between Cairns and Innisfail[21]. However, it is not known whether the current dearth of reef fishes is a direct consequence of overfishing or of the destruction of the hard coral cover of reefs by A. planci, or whether both factors have contributed. In the long term the population outbreaks could also affect tourism to Great Barrier Reef resorts. Control
of the outbreaks
Apart from attempts in the early 1960sand again in 1980 to control numbers of A. planci by hand collecting on sections of the reef at Green Island, and an ill-starred attempt to restrict the movement of A. planci on one reef by using a barrier of copper sulphate contained within a porous plastic pipe, no measures have been taken to control population outbreaks on reefs of the Great Barrier Reef. The lack of a systematic control
14
programme there contrasts markedly with the control programmes adopted in other parts of the tropical Pacific region. However, the Queensland government has legislated to confer protection on the giant triton and recently legislated to ban the use of spearguns in conjunction with SCUBA for the taking of reef fishes. It is essential that these regulations be rigidly enforced if the spectre of long-term impoverishment of reefs in the central region of the Great Barrier Reef is to be removed.
References [l] Barnes, J. H. and Endean, R. Med.J.Aust., 1,529, 1964. [2] Barnes, J. H. Amt. Nat.Hist., 15,257,1966. [3] Endean, R. ‘Report on investigations made into aspects of the current Acanthaster planci (crown-of-thorns) infestations of certain reefs of the Great Barrier Reef.’ Fisheries Branch, Department of Primary Industries, Brisbane, 1969. [4] Pearson. R. G. and Endean, R. Queensland Fish. Notes, 3, 27, 1969. [5] Endean, R. and Chesher, R. H. Biol. Conserv. 5, 87, 1973. [6] Hayashi, K. and Tatsuki, T. BulLMar. Park ResStations, 1, 11, 1975. [7] Endean, R. and Stablum, W. Atoll Res. Bull., 167, 1, 1973. [8] Idem. Atoll Res.Bull., 168, 1, 1973. [9] Idem. Environ. Conserv., 2,247, 1975. [lo] Endean, R. ‘Proc. 2nd Intl. Sympos. Coral Reefs’, 1,563,1974. 1111Chesher, R. H. in ‘Acanthaster planci: Impact on Pacific Coral Reefs’. Westinghouse Elec.^ Corp. Report to U.S. Dept. Interior. Dot. No. PB187631.0.1. 1969. [12] Ormond, R. F. G. and Campbell, A.C. ‘Proc. 2nd Intl. Sympos. Coral Reefs’, 1,595, 1974. [13] Talbot, F. H. and Talbot, M. S. Endeavour, 30,38, 1971. [14] Endean, R. ‘Proc. 3rd Intl. Sympos. Coral Reefs’, 1, 185,1977. [15] Vine. P. J. Nature Lond. 228, 341, 1970. [16] Pearson, R. G. in ‘Crown-of-thorns Starfish Seminar Proceedings’, p. 131. Australian Government Publishing Service, Canberra, 1975. [17] Watt, K. W. F. in ‘Dynamics of Populations’ (den Boer, P. J. and Gradwell, G. R. (eds) ) p.568. Centre for Agricultural Publishing and Documentation (Pudoc), Wageningen, 1970 [18] Frankel, E. Atoll Res. Bull., 220,76, 1978. [19] Endean, R. in ‘Biology and Geology of Coral Reefs. Vol. II. Biology 1’ (Jones, 0. A. and Endean, R. (eds) ) p.389. Academic Press, New York, 1973. [20] Endean, R. in ‘Fifth FAO/SIDA Workshop on Aquatic Pollution in Relation to Protection of Living Resources’, p.343. FAO, Rome, 1978. [21] Goeden, G. B. Aust.Fish., 3&l&1979. IL
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Indo-West Pacific region. Indeed, in the Ryukyus A. planci is called ‘America-yui’ because outbreaks were observed there for the first time during the American occupation following World War II [6]. By 1967the numbers of A. plunci on the reef at Green Island had obviously begun to decline and few could be found there in 1968. During the period of infestation the reef community had changed from one dominated by corals to one dominated by algae. There had also been a concomitant change in the fauna formerly associated with living corals leading to an obvious reduction in species diversity. Within 14-21 days after the skeletons of coral were exposed as a result of the feeding activities of A. planci, filamentous algae began to grow on the white exposed skeletons, which soon acquired a dark coating of algae. For months, the devastated reef presented a drab picture relieved only by the occasional live massive coral or patch of live branching coral bypassed by the voracious starfish. Gradually the picture changed. Coralline algae and stalked algae aswell assoft corals proliferated in many shallow-water areas. Three to four years after destruction of an area of hard coral small colonies of recolonizing hard corals were evident. Well-known opportunistic species such as Pocillopora damicornis, Seriatopora hystrix, and Stylophora pistillatu were among the first to settle. Fast-growing tabular colonies of Acropora hyacinthus then became well represented and these appeared to dominate subsequent stagesof recovery. By 1979, some 17 years after obvious damage to the hard coral cover of the reef was first observed, a good coral cover had been re-established at Green Island reef. However, it is unlikely that the climax stage in the recolonization process had been reached. In December, 1979, acting on information supplied by fishermen that Green Island reef was again under attack by A. planci, a party from the University of Queensland, led by the author: paid it a visit. Large numbers of adult and juvenile A. planci were seen (figure 1) and these were obviously causing extensive damage to the hard coral cover of the reef. Transects were run at several locations on the reef and, by using techniques applied in earlier surveys [7] [8], it was estimated that approximately 60 per cent of the hard coral cover of the reef had been recently killed by A.planci. The adult starfish population of the reef was estimated to be about
Figure 1 Specimens of crown-of-thorns starfish eating coral c thegenusAcroporaonthereefflat,GreenIsland.Januaryl981. Parts of the white skeletons of the coral are exposed.
Port
Douglas CAIRNS
*.Broadhurst
)i:k’.e
Reef
Reef :Tideway .._ .,
QUEENSLAND
Figure 2 Typical appearance of algae-covered skeletons coralsofthegenusAcroporakilledbythecrown-of-thorns starfish on the reef flat, Green Island, January 1981.
of plz rte
Reef
‘,BunkerGroup \
Figure3 Acrown-of-thorns starfish feeding on a massive hemisphericalcoralofthegenusPoritesonthereefflat,Green Island, Jannary, 1981.
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Figure4 MapofportionoftheQueenslandcoastshowingthe Great Barrier Reef region and localities mentioned
in the text.
Figure 5 Aggregations of crown-of-thorns starfish feeding on platecoraIsofthegenusAcroporaatHowieReef,Januan/,1981
11
350,000. This was possibly an underestimate, since soon afterwards the Australian Minister for Science was quoted in local newspapers as stating that government scientists estimated that approximately two million A. planci were present on Green Island reef. In January 1981 we resurveyed the reef and it was estimated that approximately 90 per cent of the hard coral cover of the reef had been killed (figure 2), and destruction of the remainder was in progress. Even large massive corals that, judging by their size, had been bypassed during the A. planci infestation in the 1960s were under attack (figure 3). Since our previous visit signs had been erected on the cay at Green Island by the Queensland government warning tourists of the danger of treading on the venomous spines of the starfish. The reefs of the Great Barrier Reef affected by the outbreaks Although population outbreaks of A. planci were
use by clam poachers who, prior to 1980, ravaged the reefs in the area. Be this as it may, reefs near these cays appear to have been among those most frequently visited by humans in the Swain Reefs complex. Most visitors taken, to the area by charter-boat operators engage in activities-such as line fishing, spear fishing, and shell collecting-that involve collecting elements of the fauna. Study of all reefs affected by the A. planci population outbreaks during the period 1962-1974 indicates the likelihood1 that1the [reefs, first affected,in each area were the ones most visited by humans. In 1975 reefs near lat. 14”s were found to be infested and in 1980 and 1981 the author and associates established that several reefs lying between lat. 16” 30’S and lat. 17” 30’S which had been infested with A. planci in the 1960s were again carrying population outbreaks of A. planci (figure 5). Biology of Acanthasterplanci
observed on several reefs near Green Island in 1962, it is A. planci is a large (up to 60 cm diameter) multi-armed not known whether the outbreaks began on all of them starfish. Its upper surface is covered with stout spines simultaneously. No outbreaks were observed on any that have given rise to its common name, the crown-ofreefs of the Green Barrier Reef prior to the 1960s. thorns starfish. Toxic saponins occur in the skin overHowever, in the period 1962 to 1974 inclusive the lying the spines and A. planci is the only venomous majority of the approximately 300 platform reefs of the starfish known. When adult, it appears to prey principally on acroporid corals and is apparently confined to coral Great Barrier Reef lying between lat. 14” 40’S and lat. 20% (figure 4) experienced such outbreaks [9]. In most reefs. It has the ability to utilize cetyl palmitate, the cases the bulk of the hard coral cover of those reefs major wax energy reserve of corals. In the past it has been regarded as a rare animal but its normal population examined was destroyed within two to four years [lo]. Tens of thousands of starfish are believed to have been density on reefs of the Great Barrier Reef was not present on a reef during an infestation. Subsequently A. known until 1972. In that year the services of about a planci disappeared from each reef, and as no mass hundred trained divers were utilized to determine mortality was observed at any stage it is assumedthat the population densities of A. planci on several uninfested starfish migrated from the devastated reefs. In a few reefs of the Great Barrier Reef that carried an apparentinstances invasion of a reef by adult A. planci arriving at ly normal coral cover. A figure of approximately 6 specimens (all mature adults) per km* was obtained [lo]. the base of the seaward slopes of a reef, presumably after migrating there from an adjacent reef, was witnes- This figure agreed well with earlier estimates for reefs in the central pacific region [ll] and for reefs in the Red sed. Occasionally only juvenile starfish were present in large numbers on a reef, but in many casesinfested reefs Sea [12]. Thus the starfish can be considered a rare, as well as a highly specialized carnivore found on coral carried both adults and juveniles. During the period 1962-1974 the principal direction of the spread of the reefs. It has been calculated that a mean density of about 14 infestations was from reefs near Cairns to others progressively further to the south [9], but this is not to imply adult specimens of the starfish per 1000m* is sufficient to kill the bulk of the hard coral cover of a reef of average that there was a front of invading starfish moving relentlessly southwards. In retrospect, it now seems size (10 km* in flat projection) in 2.5 years, during which time recolonization by hard corals is negligible. This likely that certain platform reefs, first in the region lying between the latitudes of Port Douglas and Innisfail and represents an increase by a factor of about 2,330 in the subsequently in areas further to the south and to the normal population density of A. planci on uninfested reefs. Obviously it is not resource-limited at normal north, became infested and acted as foci for the infestation of adjacent reefs, including outer platform reefs in population density. Other features of its life history that have relevance each area. Certainly reefs such as Rib Reef, Broadhurst for the present discussion are its great fecundity (each Reef, Line Reef, and Tideway Reef became infested female having the potential to release millions of eggs), before other reefs in their vicinity. A few reefs outside the region extending from lat. 14” its limited breeding season, and the presence in its life 40’S to lat. 20% became infested in the period 1962- cycle of planktotrophic larval stages of long duration. After settlement and metamorphosis juveniles eat cora1974. Some of them were lagoon reefs in the Bunker line and other epiphytic algae. They grow rapidly and at Group near the southern end of the Great Barrier Reef. an age of 4-5 months they resemble miniature adults and Others were located in the Swain Reefs complex [lo]. have adopted adult feeding behaviour. When one year The initial infestation in the Swain Reefs complex involved reefs near Lavers Cay (approximately lat. 21” old they are 6 to 7 cm in diameter. A diameter of 20 cm is 10’S) and Mystery Cay (approximately lat. 21” 20’S) reached by specimens aged between 1% to 2 years. Specimens become sexually mature when 14-16 cm in which are among the most remote reefs of the Great Barrier Reef. However, charter-boat operators use diameter. The age attained by large specimens of A. these cays as aids in navigating the labyrinthine maze of planci is not known, but is certainly in excess of five years. reefs in the area, and no doubt they were put to a similar 12
Mortality at different stages in the life history is not known. Predators of juvenile A. plunci on reefs in Great Barrier Reef waters include xanthid crabs and the groper, Promicrops lanceolatus. Known predators of, adult starfish on the Great Barrier Reef include the giant triton, Charonia tritonis and the large wrasse, Cheilinus undulatus. Although large adults frequently lose one or more arms to predators on reefs they appear to survive such attacks. It is possible that other reef fishes are also predators of juvenile and/or adult starfish. Certain puffer fishes and trigger fishes have been shown to be predators of adult A. planci in the Red Sea [12]. Possible causes of the outbreaks
Despite a considerable amount of research since a previous review [13] in this journal in 1971 of the A. plunci problem on the Great Barrier Reef, it is still not possible to state the cause or causes of the population outbreaks. The various hypotheses that have been proposed to account for the outbreaks fall into two groups. Those in one group might be termed the normal event hypotheses, and those in the other the abnormal event hypotheses. Many of those belonging to the first group can be readily refuted [14]. Others which relate to natural fluctuations in the breeding successof A. plunci [15][16] are more difficult to refute. Because the starfish has a high fecundity and planktotrophic larval stages, environmental conditions could be more conducive to the production and survival of large numbers of larvae in some years than in others. Infestations of reefs could occur in the years in which large numbers of larvae are recruited. However, the A. plunci population structures found on infested reefs of the Great Barrier Reef were usually polymodal, indicating the existence of several year classes[7]. Further, the infestations have continued since the early 1960s.All this renders it unlikely that the outbreaks could be the direct result of exceptional recruitment in one particular year or even in a number of successive years. Then, too, it has become apparent that, at any one time, some reefs in a particular area may suffer population outbreaks while others in the same area may not. This suggeststhat the infestations are not necessarily the result of abnormally large numbers of larvae being present in the plankton at a particular time. Rather does it suggestthat some reefs are more prone to infestation than others in the same area. None of the normal event hypotheses indicate why this should be so. There remain the hypotheses that the A. plunci population outbreaks are abnormal events. K. W. F. Watt [17] has written that ‘It should be noted that a great many of the species in the world are so rare that they have attracted little attention, and also may be quite stable in numbers which would also prevent them from attracting attention’. Prior to the middle of this century A. planci appears to have been such a rare species. There is an absence of scientific or historical records providing unequivocal evidence of A. planci infestations of reefs prior to the 1950s although the venomous nature of the species was well known to the indigenous peoples of the tropical West Pacific region. The discovery of Acanthaster debris in sediments on several reefs of the Great Barrier Reef [18] was claimed to be evidence of previous ‘plagues’ of the starfish on these reefs. However, information was not provided on how
many skeletal remains of A. planci per kg of sediment represent a past ‘plague’. The apparent absence of any mass mortality among starfish present on a reef during an infestation raises problems in interpreting the significance of the debris. Difficulties are also encountered in accounting for the retention of Acanthuster debris on platform reefs which reached the surface hundreds of years ago and which are growing on antecedent knolllike structures. As already noted, A. plunci has the attributes of a rare and specialized carnivore belonging to the coral reef community. These communities are regarded by many biologists as having a particularly stable or predictable organization because they possessnumerous homeostatic mechanisms which buffer any tendency for marked change in the population densities of constituent species. In the case of A. plunci only a modest increase in the normal population density of the species is required to obliterate the basic element of the coral reef community, the hard coral cover. Obviously, the number of starfish present must normally be regulated within narrow limits. The fact that population outbreaks have occurred suggests that a perturbation of a novel kind with which existing homeostatic mechanisms cannot cope, or which entirely disrupts these mechanisms, has been introduced into the system. What is this perturbation? The observation that infestations appear to have begun on the Great Barrier Reef and elsewhere [5] on accessible reefs visited by humans suggests human involvement in initiating them. It is difficult to perceive a mechanism whereby human activities could increase the success of recruitment of larval A. planci to a reef. Pollution, by selectively eliminating larval predators, comes to mind but should affect recruitment of A. planci to all reefs in any area rather than affecting one or a few reefs. Then again, pollution could hardly be involved in facilitating recruitment to remote reefs in the Swain Reefs complex. If attention be concentrated on the possibility that human activities might have an effect on part-larval starfish populations, then a mechanism for the population outbreaks suggestsitself. Since neither adult nor juvenile starfish are resource limited when present on reefs at normal population density, it seems likely that their populations are normally controlled by predators. Release of predator pressure on post-larval stages as a result of human activity could be a key factor in triggering the infestations. Because their size, venomousness, and ability to regenerate missing parts render large adult starfish less vulnerable to predators than juveniles and small adults, predation on juveniles and small adults could have greater significance than predation on large adults. The giant triton, Charonia tritonis, is an important predator on large juvenile and small adult A. planci, and gropers (Promicrops lanceolatus) are known to prey on juvenile A. planci. Evidence has been obtained of an extensive trade in giant tritons in Great Barrier Reef waters and many reefs there have been overfished, particularly by spear-fishermen [19] [20]. Excessive collecting by humans of giant tritons and resident reef fishes, especially groper, could well have been responsible for initiating the A. planci outbreaks. Such an hypothesis is in accord with the history of the population outbreaks, with their locations, and with the views of many biologists on the 13
organization of coral reef communities. Moreover, it should be possible to test the hypothesis in the field. Possible consequences
of the outbreaks
It is believed that the bulk of the hard coral cover of the majority of platform reefs in the central region of the Great Barrier Reef was devastated by A. planci population outbreaks during the 1960s and 1970s. The longterm ecological consequences of the destruction of this huge amount of coral are difficult to predict. Particularly is this so because population outbreaks are now reoccurring on these reefs as their hard coral cover is re-established. It seems likely that the factors which have triggered the original outbreaks are still operative. This could lead to impoverishment for decades of reefs in the central region of the Great Barrier Reef. Furthermore, infestations are now occurring on some reefs to both the north and south of the central region. This suggests that the perturbations responsible for the infestations are now operating outside the central region and opens up the possibility that the whole Great Barrier Reef ecosystem could ultimately be affected. As well ashaving serious ecological consequences, the A. planci population outbreaks could have serious economic consequences. Several workers who have studied the phenomenon have commented on the dearth of resident fishes on reefs affected by the population outbreaks. It is of interest to note that commercial fishing for reef-associated fishes has now virtually ceased on reefs between Cairns and Innisfail[21]. However, it is not known whether the current dearth of reef fishes is a direct consequence of overfishing or of the destruction of the hard coral cover of reefs by A. planci, or whether both factors have contributed. In the long term the population outbreaks could also affect tourism to Great Barrier Reef resorts. Control
of the outbreaks
Apart from attempts in the early 1960sand again in 1980 to control numbers of A. planci by hand collecting on sections of the reef at Green Island, and an ill-starred attempt to restrict the movement of A. planci on one reef by using a barrier of copper sulphate contained within a porous plastic pipe, no measures have been taken to control population outbreaks on reefs of the Great Barrier Reef. The lack of a systematic control
14
programme there contrasts markedly with the control programmes adopted in other parts of the tropical Pacific region. However, the Queensland government has legislated to confer protection on the giant triton and recently legislated to ban the use of spearguns in conjunction with SCUBA for the taking of reef fishes. It is essential that these regulations be rigidly enforced if the spectre of long-term impoverishment of reefs in the central region of the Great Barrier Reef is to be removed.
References [l] Barnes, J. H. and Endean, R. Med.J.Aust., 1,529, 1964. [2] Barnes, J. H. Amt. Nat.Hist., 15,257,1966. [3] Endean, R. ‘Report on investigations made into aspects of the current Acanthaster planci (crown-of-thorns) infestations of certain reefs of the Great Barrier Reef.’ Fisheries Branch, Department of Primary Industries, Brisbane, 1969. [4] Pearson. R. G. and Endean, R. Queensland Fish. Notes, 3, 27, 1969. [5] Endean, R. and Chesher, R. H. Biol. Conserv. 5, 87, 1973. [6] Hayashi, K. and Tatsuki, T. BulLMar. Park ResStations, 1, 11, 1975. [7] Endean, R. and Stablum, W. Atoll Res. Bull., 167, 1, 1973. [8] Idem. Atoll Res.Bull., 168, 1, 1973. [9] Idem. Environ. Conserv., 2,247, 1975. [lo] Endean, R. ‘Proc. 2nd Intl. Sympos. Coral Reefs’, 1,563,1974. 1111Chesher, R. H. in ‘Acanthaster planci: Impact on Pacific Coral Reefs’. Westinghouse Elec.^ Corp. Report to U.S. Dept. Interior. Dot. No. PB187631.0.1. 1969. [12] Ormond, R. F. G. and Campbell, A.C. ‘Proc. 2nd Intl. Sympos. Coral Reefs’, 1,595, 1974. [13] Talbot, F. H. and Talbot, M. S. Endeavour, 30,38, 1971. [14] Endean, R. ‘Proc. 3rd Intl. Sympos. Coral Reefs’, 1, 185,1977. [15] Vine. P. J. Nature Lond. 228, 341, 1970. [16] Pearson, R. G. in ‘Crown-of-thorns Starfish Seminar Proceedings’, p. 131. Australian Government Publishing Service, Canberra, 1975. [17] Watt, K. W. F. in ‘Dynamics of Populations’ (den Boer, P. J. and Gradwell, G. R. (eds) ) p.568. Centre for Agricultural Publishing and Documentation (Pudoc), Wageningen, 1970 [18] Frankel, E. Atoll Res. Bull., 220,76, 1978. [19] Endean, R. in ‘Biology and Geology of Coral Reefs. Vol. II. Biology 1’ (Jones, 0. A. and Endean, R. (eds) ) p.389. Academic Press, New York, 1973. [20] Endean, R. in ‘Fifth FAO/SIDA Workshop on Aquatic Pollution in Relation to Protection of Living Resources’, p.343. FAO, Rome, 1978. [21] Goeden, G. B. Aust.Fish., 3&l&1979. IL
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