Chapter 3. Habitat
The spatial distribution of coral-reef starfish has been studied at several different scales. The physical, biological and historical parameters that explain the distribution of these species on the global scale (Clark and Rowe, 1971) will not directly explain the spatial pattern of an assemblage on a single reef. The small-scale distribution of Linckia laevigata on the fringing reef at Guam, and some factors which determine the abundance of this species in different habitats, were described by Strong (1975). The distribution and movements of Linckia laevigata at Lizard Island were examined by Thompson and Thompson (1982). Laxton (1974) suggested that Linckia laevigata may alter its distribution following outbreaks of Acanthaster planci. The distribution of an assemblage of starfish on a reef that is not known to have undergone outbreaks of Acanthaster planci has not been studied previously.
Feeding of starfish was extensively reviewed by Sloan (1980) and Jangoux (1982) and there have been many detailed examinations of the diets, competitive interactions and niche separation of colder water species (Blankley, 1984; Menge, 1972 a, 1972 b, 1981; Menge and Menge, 1974). The ecology of the tropical omnivorous, Atlantic species Oreaster reticulatus has been extensively studied by Scheibling (1980, 1981 a, b, 1982). The known diets and habitat preferences of the Indo-West Pacific coral-reef species have been tabled by Yamaguchi (1975 b). The contribution of these aspects of niche specialisation to the co-existence of many asteroid species in the coral reef ecosystem is poorly understood.
The general correlation between food supply and growth in asteroids has been discussed (Mead, 1900; Wolda, 1970; Paine, 1976). Species such as Acanthaster planci and Culcita novaeguineae are known to prey on hard corals (Endean, 1969; Yamaguchi, 1975 b; Glynn and Krupp, 1986). The response of Acanthaster planci to different prey species has been studied (Ormond, Hanscomb and Beach, 1976). Asterina anomala, Asterina burtoni, Ophidiaster granifer and Gomophia egyptiaca are known to feed on sponges and ascidians (Thomassin, 1976; Yamaguchi, 1975 b) while Astropecten polyacanthus and other members of its genus are known to prey on molluscs (Christensen, 1970; Ribi and Jost, 1978; Jost, 1979). Coscinasterias calamaria along with most members of the Order Forcipulatida, which are primarily inhabitants of temperate waters, are known to also prey on molluscs (Sloan, 1980; Jangoux, 1982).
However, the vast majority of coral-reef starfish are thought to be general detritovores and to feed primarily on the epibenthic felt (Thomassin, 1976) which is widely distributed throughout the reef environment. The possibility of ciliary nutrition (filter feeding) in some asteroids was raised by Gemmill (1915).
With the exception of what were once considered “primitive” genera such as Astropecten and Luidia (see Blake, 1987), starfish generally feed by everting their stomach over the substrate and digestion is external (Blake, 1990). However, the forcipulate species Heliaster helianthus is known to possess a flexible feeding habit involving both intra-oral and extra-oral feeding (Tokeshi, 1991). When Acanthaster planci and Culcita novaeguineae feed on hard coral they evert their stomachs and leave white feeding scars where the living tissue has been digested off the skeleton (Yamaguchi, 1975 b). Predominantly epibenthic feeders such as members of the genera Linckia, Nardoa and Ophidiaster leave no such feeding mark to indicate the position of their everted stomach when they are removed from the substrate while feeding (Yamaguchi, 1975 b).
While there have been extensive studies of the micro-habitat requirements of some coral-reef animals, for example gastropods (see e.g. Kohn and Leviten, 1976; Leviten and Kohn, 1980; Reichelt, 1982) there has been little work done on this aspect of coral-reef asteroid ecology. The role of habitat complexity in determining the population densities of species of gastropod within the coral reef ecosystem was discussed by Kohn (1968). However, the temporal scale of many community studies is often insufficient to determine the stability, or otherwise, of the observed community structure.
The degree to which species specialise in their use of habitat and other resources is a major component of the complexity of any assemblage (Klopfer, 1959; Klopfer and MacArthur, 1960, 1961; MacArthur and Levins, 1964, 1967; May and MacArthur, 1972. Reichelt (1982) regarded the availability of refuges from predation, desiccation and turbulence as determining factors in the spatial pattern of many intertidal species of gastropod. Kohn (1968) suggested that habitat complexity and the resultant spatial heterogeneity may directly determine the diversity of species assemblages.
Other authors have stated that the species assemblages that they examined were predominantly random. Guilds of species which use their habitat in a similar fashion were proposed by Sale (1976, 1977). In determining the spatial distribution of organisms, many authors propose the use of null (or neutral) models to prevent random events from being misinterpreted as meaningful biological pattern (Connor and Simberloff, 1979; McGuinness, 1984). However, caution over the misuse of inappropriate null models, which incorrectly reject real pattern, has been suggested by other authors (Dunbar, 1980; Quinn and Dunham, 1983; Roughgarden, 1983; Gilpin and Diamond, 1982).
At the completion of each traverse, all specimens were identified, counted and measured. The estimated area of the traverse was also recorded. While traverses were not stratified with respect to habitat, the zone of maximum density (primary habitat) was quite apparent for some species. Where a species occurred in more than one zone, the zones of less-frequent occurrence were referred to as secondary habitats. The distinction between primary and secondary habitat was much clearer in some species than in others. Some species were found so rarely that their range of habitat is unknown. In these cases, the zone in which they were located is regarded as the primary habitat.
25 specimens of Linckia laevigata were tagged with small plastic clothing tags which were inserted through the body wall of one arm, near its base, in such a way that a number inscribed on each tag was visible on close examination of the specimen. These starfish were then released at a site that provided no refuge other than under boulders. All boulders within a radius of 30 meters were overturned during attempts made to relocate them at 24 hour intervals. Twenty-five specimens of each of five additional species, Linckia guildingii, Linckia multifora, Nardoa novaecaledoniae, Nardoa pauciforis and Echinaster luzonicus, were released following similar tagging. Other methods of tagging, such as stains (Loosanoff, 1937; Feder, 1955; Vernon, 1937), were not successful because of low intensity of staining.
The feeding of starfish at Heron Reef was not examined in detail. When starfish specimens were collected, their stomachs were often found everted over the substrate. The approximate size of the stomach was noted along with the type of food material on which they appeared to be feeding. Any mark that their feeding activity may have left on the surface of the substrate was recorded.
Culcita novaeguineae did not occur commonly in any habitat that was sampled by the shallow-water traverses. This species appeared to be more abundant in coral pools adjacent to the lagoon than on either the reef crest or reef flat at the western end of the reef. Linckia guildingii, Linckia laevigata, Nardoa novaecaledoniae and Nardoa pauciforis appeared to be slightly more abundant in one zone (primary habitat) than another (secondary habitat), but this difference was not clear, and was not quantified. All the remaining species occurred with either much greater densities in their primary habitats compared with their densities in secondary habitats, or were found in only one major zone.
The species that are regarded as exposed sometimes were found under boulders or coral rubble but no regular pattern of concealment was apparent in these species. The cryptic species varied in their type of refuge, which ranged from small rubble to large boulders.
The primary (1′) habitat, secondary (2′) habitat and general pattern of concealment of each species are listed in Table 3.1. These data are not quantitative but represent a general impression of the overall distribution pattern for each species. While some species are extremely restricted in their spatial distribution, others are widespread and it was not possible to estimate the abundance of each species, in each zone, in each sampling period when specimens were primarily required for size-frequency and reproductive analysis.
The general location of each species at Heron Reef and the known diet of each of the species (after Yamaguchi, 1975 b) are listed in Table 3.2. While diet was not studied in detail, observations made during this study confirm those of Yamaguchi that most species of starfish feed on epibenthic felt.
Table 3.1 The species of Asteroidea, primary habitat, secondary habitat, and their habit (excluding those species that occur predominantly in the off-reef floor zone).
SPECIES 1′ HABITAT 2′ HABITAT HABIT
Astropecten polyacanthus floor flat exposed Iconaster longimanus slope floor exposed Culcita novaeguineae flat crest, slope exposed Acanthaster planci slope flat both Asteropsis carinifera crest cryptic Dactylosaster cylindricus crest cryptic Fromia elegans slope crest exposed Fromia milleporella crest exposed Gomophia egyptiaca slope crest both Linckia guildingii flat crest exposed Linckia laevigata flat crest exposed Linckia multifora crest slope both Nardoa novaecaledoniae crest flat exposed Nardoa pauciforis flat crest exposed Nardoa rosea floor flat exposed Neoferdina cumingi slope crest both Ophidiaster armatus floor crest exposed Ophidiaster confertus crest cryptic Ophidiaster granifer crest cryptic Ophidiaster lioderma crest cryptic Ophidiaster robillardi crest cryptic Ophidiaster watsoni crest cryptic Anseropoda rosacea flat cryptic Asterina anomala crest cryptic Asterina burtoni crest cryptic Disasterina abnormalis crest cryptic Disasterina leptalacantha flat crest cryptic Tegulaster emburyi crest cryptic Mithrodia clavigera crest exposed Echinaster luzonicus crest flat, slope both Coscinasterias calamaria crest cryptic
Diet and location of each species (excluding those species that occur predominantly in the off-reef floor zone). In some species the diet is unknown. asc = ascidian
SPECIES DIET LOCATION Astropecten polyacanthus mollusc fine sand 0-30 m Iconaster longimanus felt rubble 20-30 m Culcita novaeguineae coral, felt sand, rubble 0-25 m Acanthaster planci coral live coral 0-25 m Asteropsis carinifera - sand under rock Dactylosaster cylindricus - rock under rock Fromia elegans felt rubble 0-25 m Fromia milleporella - rubble Gomophia egyptiaca sponge, asc sand, rubble 0-20 m Linckia guildingii felt sand, rubble Linckia laevigata felt sand, rubble Linckia multifora felt attached under rock Nardoa novaecaledoniae felt sand, rubble Nardoa pauciforis felt sand, rubble Nardoa rosea - sand, rubble 0-30 m Neoferdina cumingi - sand, rubble 0-20 m Ophidiaster armatus - sand, rubble 0-30 m Ophidiaster confertus - rock under rock Ophidiaster granifer sponge, asc attached under rock Ophidiaster lioderma - rubble under rock Ophidiaster robillardi - attached under rock Ophidiaster watsoni - under boulder Anseropoda rosacea - sand Asterina anomala sponge, asc attached under rock Asterina burtoni sponge, asc attached under rock Disasterina abnormalis felt attached under rock Disasterina leptalacantha felt attached under rock Tegulaster emburyi - attached under rock Mithrodia clavigera - rubble Echinaster luzonicus felt sand, rubble 0-25 m Coscinasterias calamaria mollusc attached under rock
In all species, excepting Acanthaster planci, the stomach was small, usually about the same area as the disc. At no time was the ingestion of large food material observed in any species but Astropecten polyacanthus and Coscinasterias calamaria were occasionally observed feeding on very small gastropods which were partially inside the mouth. In all other species the feeding was entirely extra-oral.
When the stomach was everted, the oral spines were oriented away from the mouth and both digestion and absorption occurred outside the body. At the completion of feeding, the stomach was withdrawn through the mouth and the oral spines were reoriented such that they occluded the mouth opening. All species commenced retraction of the stomach when removed from the substrate but the delay, before retraction was complete, varied from a few seconds in the case of epibenthic felt feeders with small stomachs to a few minutes in the case of Acanthaster planci. In all species, the oral spines could not reorient into the non-feeding (defensive) positions until the stomach was fully retracted inside the mouth.
The only two species which left feeding scars on the substrate were Culcita novaeguineae and Acanthaster planci. Both of these species feed on hard coral. Culcita novaeguineae was observed also feeding on bryozoan colonies at the base of the reef slope at a depth of 20 meters. All the other species had not altered the appearance of the substrate on which they had been feeding. Fromia elegans, Linckia guildingii, Linckia laevigata, Linckia multifora, Nardoa novaecaledoniae, Nardoa pauciforis, Disasterina abnormalis, Disasterina leptalacantha and Echinaster luzonicus were only observed to evert their stomach over substrate of either sand or coral-rock that was covered with a fine layer of organic material (epibenthic felt). Ophidiaster granifer and Asterina burtoni were observed with their stomachs everted over both solitary and colonial ascidians, but these two species also everted their stomachs over the epibenthic felt.
The results of movement studies of Linckia laevigata showed that this species is capable of moving at least 30 meters in a 24 hour period. Only 12 out of 25 specimens, which were released on coral rubble substrate at the outer, northern reef flat were able to be relocated 24 hours later. Eight specimens had not moved, three specimens had moved one meter, one specimen had moved 15 meters, but 13 specimens had moved a distance greater than 30 meters, and were not relocated. After a further 24 hours only two tagged specimens and no untagged specimens could be relocated in the vicinity of the point of release. Of the 25 specimens of six other species that were released following tagging, no tagged specimens were observed when attempts were made to relocate them after an interval of two months. It is possible that the small plastic tags were lost from the arms of these specimens.
It can be seen from Table 3.1 that 16 of the 31 asteroid species recorded from Heron Reef were found in more than one of the major coral reef zones during this study. Echinaster luzonicus was found in all zones. The less common species were not encountered often enough for the data to show their complete distribution. With the exception of Culcita novaeguineae, Linckia guildingii, Linckia laevigata, Nardoa novaecaledoniae, Nardoa pauciforis and Echinaster luzonicus, the asteroids at or in the vicinity of Heron Reef can be divided into reef flat, reef crest, reef slope and off-reef floor species.
Species that occurred with their highest abundance on the reef flat are Culcita novaeguineae, Linckia guildingii, Linckia laevigata, Nardoa pauciforis and Disasterina leptalacantha. All species, excepting D. leptalacantha, are a large size when fully grown (large-bodied) and lie fully exposed in the daytime. However, they might complete their early development under boulders on the reef crest (Yamaguchi 1973 a, b). Disasterina leptalacantha is a small cryptic species found occasionally on the reef crest, or more often, under slabs of beachrock on the innermost part of the reef flat.
Linckia multifora, Nardoa novaecaledoniae and Echinaster luzonicus occurred with highest abundance on the reef crest. Species which were found exclusively on the reef crest are Asteropsis carinifera, Dactylosaster cylindricus, Fromia milleporella, Ophidiaster confertus, Ophidiaster granifer, Ophidiaster lioderma, Ophidiaster robillardi, Asterina anomala, Asterina burtoni, Disasterina abnormalis, Tegulaster emburyi, Mithrodia clavigera and Coscinasterias calamaria.
Predominantly reef slope species are Iconaster longimanus, Fromia elegans, Gomophia egyptiaca, Neoferdina cumingi and Acanthaster planci. Their distribution seems more closely allied to living coral than is that of the species which inhabit the reef flat or reef crest.
The off-reef floor is not a true coral reef environment although numerous solitary corals and alcyonarians occur. The asteroid fauna of this environment is made up chiefly of the widespread sub-littoral species Astropecten polyacanthus, Pentaceraster regulus and Euretaster insignis in the deeper water (30-40 meters). Nardoa rosea, Ophidiaster armatus, Tamaria megaloplax, Echinaster stereosomus and large individuals of Linckia multifora and Echinaster luzonicus are found in the shallower water (20-30 meters) near the base of the reef slope.
Of the 25 starfish species found on Heron Reef itself, 17 were located only in intertidal regions and an additional three were found predominantly in intertidal regions. The other five species have been found intertidally, but occur predominantly in subtidal habitats.
Some cryptic reef crest species such as Asteropsis carinifera, Linckia multifora, Disasterina abnormalis, Echinaster luzonicus and Coscinasterias calamaria occur under rocks which possess a sparse development of epibiota. This would appear to be a short lived micro-habitat. Other cryptic reef crest species such as Gomophia egyptiaca, Ophidiaster granifer, Ophidiaster robillardi, Asterina anomala and Asterina burtoni are more frequently associated with encrustations of sponges and ascidians (Yamaguchi, 1975 b). Ophidiaster confertus was found either under or attached to the side of large boulders on the reef crest. Other species such as Dactylosaster cylindricus, Neoferdina cumingi, Ophidiaster lioderma and Tegulaster emburyi were not located in sufficient numbers to establish any pattern of occurrence. The reef crest species, that are regarded as cryptic during the day, did not move into exposed locations at night and species could remain cryptic during periods of activity. The reef crest, interstitial environment which is composed of highly fragmented coral, continually percolated by sea water, might provide refuges from desiccation and predation for some species but all attempts to locate asteroids in this micro-habitat were unsuccessful.
The epibenthic felt which covers large areas of intertidal coral reef habitat is composed primarily of protozoans, algae and bacteria (Thomassin, 1976). At Heron Reef and on other reefs, this appears to be a substantial resource. It would be of interest to know if competitive exclusion of one or more species can occur when population densities are higher than those recorded at Heron Reef. The role of species specific enzymes in the digestion of different organisms composing the epibenthic felt has not been investigated to date. Each species might possesses enzymes which facilitate the efficient exploitation of a different component of the epibenthic felt. A biochemical study of the gastric mucosa of each asteroid species would be needed to establish resource partitioning on this microscopic scale.
The feeding and movements of Acanthaster planci was studied by Keesing and Lucas (1992). This species has been shown to possess an enzyme which can efficiently digest the wax ester, Cetyl Palmitate, which is stored in the soft tissues of hard corals (Benson et al., 1975; Brahimi-Horn, 1989). Consequently, this asteroid must be regarded as a highly specialised predator of scleractinians. It is possible that other highly specialised enzymes occur in coral-reef asteroids. To exploit epibenthic felt efficiently, a scavenger would utilise mechanical or bacterial breakdown of algal cell walls and in other taxa this would be accomplished within a gut and the freed inter-cellular material would be subsequently assimilated by the organism. The epibenthic feeding asteroids evert their stomach over the felt and digestion occurs externally. These asteroids rely on enzymes to complete the digestion process but there are few known eucaryote enzymes which are capable of chemically digesting cellulose walls of algae. Diatoms, which are common in the epibenthic felt, have siliceous walls and the chemical digestion of this material, by any organism, would seem impossible. It is apparent, however, that many species of asteroid coexist on this same resource and further work is needed on possible dietary (enzyme) specialisation.
Predation on molluscs has been recorded in Astropecten polyacanthus and Coscinasterias calamaria. The paucity of mollusc-feeding coral-reef asteroids on Heron Reef is noticeable, compared with their high abundance in temperate waters (see Menge, 1975; Kwon and Cho, 1986; Nojima et al., 1986). Individuals of Coscinasterias calamaria found in the reef crest habitats were only small (R <20 mm), as were the gastropod prey on which they were observed feeding. the mobility of starfish might be insufficient to allow large-scale foraging on a coral reef as well as sufficient aggregation for successful reproduction.
Blake (1983) suggested that the general body plan of molluscivorous starfish leaves them vulnerable to predators. The observed delay in oral spine relocation following the commencement of stomach retraction, together with the defensive nature of these spines, suggests that the oral region of a starfish may be especially vulnerable to predatory attack particularly during and immediately following starfish feeding. The absence of adult specimens of Coscinasterias calamaria and other molluscivorous species of starfish may be related to the dangers inherent in this type of feeding.
In summary, the coral-reef starfish that occurred at Heron Reef showed some inter-specific variation with respect to diet, but many species appeared to feed on the same food (epibenthic felt). These species also showed some inter-specific variation with respect to habitat, but in every coral reef zone, some species sought no refuge and occurred with exposed habits. Of the species that occur predominantly on coral reefs, clear examples of niche (dietary or microhabitat) specialisation are known only for Culcita novaeguineae and the predominantly subtidal species Acanthaster planci. Clear examples of competitive interactions were not observed during this study.