coral reefs can be divided into grazers, etchers and borers. Each of these groups .... injested pieces of calcium carbonate into a fine paste. Parrotfish are able to ...
Coral Reefs
Coral Reefs (1986)4:239-252
O Springer-Verlag 1986
Biological destruction of coral reefs A review P.A. Hutchings The InvertebrateDivision,The AustralianMuseum,6-8 CollegeStreet,Sydney,N. S.W. 2000,Australia Accepted20 January 1986 Abstract. The major agents of biological destruction of coral reefs can be divided into grazers, etchers and borers. Each of these groups is reviewed on a world wide basis, together with the mechanisms by which they destroy the coral substrate. Rates of bioerosion attributed to major agents of grazers, etchers and borers are given, together with limitations of some of the measurements. Recent work is highlighting the variability in rates of bioerosion both over time and space. Factors which may be responsible for this variability are discussed. Bioerosion is a major factor influencing reef morphology and the ways in which this is achieved is discussed in some detail. Although the review concentrates mainly on present day reefs, some attempt is made to consider the impact of bioerosion on older reefs.
Introduction The structure and form of ancient and modern coral reefs is the result of the interaction between reef growth and reef destruction. Reef growth has received much attention particularly in terms of physical characteristics and patterns of coral zonation. Reef destruction by comparison has received scant attention yet boulder tracts, eroded reef flats, cay and lagoonal sediments are visible reminders that destructive processes are continually operative and are substantially affecting reef growth (Davies 1983). The agents of destruction are biological, physical and chemical; a compartmentalisation which implies that they act separately. In fact, they are intimately related. Biological agents of destruction often weaken the substrate and make it more susceptible to physical and chemical erosion and certainly the reverse situation occurs where damage caused by physical or chemical erosion facilitates bioerosion. The purpose of this review is to collate and synthesise existing data on biological destruction of reefs. A partial view of this subject has been made by Davies (1983).
I. Agents and processes of biological destruction of coral reefs Agents of destruction can be divided into grazing, etching and boring. Although they are treated separately here some overlap occurs and the distinction may be somewhat artificial. Two processes of biological destruction occur, chemical dissolution of the substrate and the mechanical abrasion of the substrate, and again these are not mutually exclusive. In many cases the complete process is not fully understood.
a) Grazing The principal grazers of coral reef substrates are echinoids and a wide variety of fish. They graze live or dead coral substrates, encrusting coralline algae, tufted or filamentous algae growing on hard reef substrates in search of food, or in some cases to etch a home scar or cavity to which they return after foraging to give them protection from dislodgement by predators or wave action. However, in some cases algae may be grazed without the loss of CaCO 3. Bardach (1961) lists seven families of West Indian fish whose intestinal tracts consistently contained large amounts of calcium carbonate. Some, for example the mullids (goatfish), accidently ingest sediment in their search for food (Frydl and Stearn 1978). Others such as tetradontids (pufferfish) bite and swallow the tips of growing corals (Cloud 1959). Acanthurids (surgeonfish) and scarids (parrotfish) scrape the surface with their teeth, producing new sediment. Although the erosive effects of parrot fish on carbonate substances has been known since the work of Darwin (1845), there has been considerable controversy in the literature concerning the extent to which these fish ingest living coral skeletal material in comparison to loose sediment such as sand. Several recent studies both in the Caribbean (Randall 1967; Gygi 1975) and on the Great Barrier Reef (Stephenson and Searles 1960; Randall 1974; Choat 1966, 1983; Russ 1984a, b) on the gut contents and behaviour
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of scarids have suggested that they graze on the soft algae growing on dead coral surfaces and rarely attack living corals or clean dead substrates. However, in the process of removing the algae, they also remove a surface veneer of the coral substrate. More recently, a comprehensive study on several species of parrot fish by Frydl (1977) and Frydl and Steam (1978) in Barbados has shown that they both ingest sand and scrape and bite offmaterial from the surface of dead and live coral and rubble. Thus they recycle "old" sediment and probably break it down further. They also produce new sediment and erode the reef. The proportion of "old" to "new" sediment varies according to the species of fish. A breakdown of these figures from Barbados is provided by Scoffin et al. (1980). Parrotfish grazing on dead coral substrates at Lizard Island, Great Barrier Reef, show distinct preferences for particular habitats such as lagoonal patch reefs (Choat 1983). The grazing marks can be assigned to particular species (Bellwood personal communication). Both parrotfish and surgeonfishes have an alimentary tract which is well adapted to carbonate ingestion. Parrotfishes have massive parrot like beaks of fused teeth for cropping the substratum, sets of pharyngeal bones which act as mills for grinding sediment and algae, and have no stomachs (A1-Hassaini 1945; Schultz 1958; Gohar and Latif 1963). By contrast surgeonfishes have less massive but still well adapted dentition, lack pharyngeal mills and have well developed stomachs which in grazing species effectively form a thick walled gizzard (Jones 1968). The gizzard of surgeonfish and the pharyngeal mill of parrotfish have a similar function, that is to grind the injested pieces of calcium carbonate into a fine paste. Parrotfish are able to dissolve calcium carbonate in their gut and Smith and Paulson (1974, 1975) have suggested that during this dissolution, nutritionally important organic material is released from the calcium carbonate matrix which can then be absorbed through the gut wall. As well as providing nutrition the dissolved material contributes to the CO2 load existing on the CO2 transport mechanism of the fish. Parrotfish have evolved ways of physiologically coping with the additional CO2 loads, suggesting that they have been eating and dissolving CaCO3 for a long time. Parrotfish have been recognised in Eocene deposits laid down in shallow tropical seas, suggesting a long association between these fish and coral reefs. Echinoids are major eroders of coral reefs at least in the Caribbean and on some eastern Pacific reefs where high population densities occur. Diadema antillarum occurs at densities of up to 23 per m 2 on Barbados fringing reefs (Hunter 1977; Stearn and Scoffin 1977). Higher densities have been recorded on reefs at Discovery Bay, Jamaica, where Sammarco (1982) found Echinometra in densities of 50/m 2. Far lower densities occur on the Great Barrier Reef although no density figures seem currently available. The high densities of echinoids reported from the Caribbean are mainly from heavily overfished reefs and much lower densities are typically recorded from un-
fished or lightly fished reefs (see Table 2, of Hay 1984), suggesting a positive correlation between urchin densities and fishing pressure. Thus on non-disturbed Caribbean reefs, echinoid grazing will not have the same impact as on disturbed reefs. In the Galapagos Islands, Glynn et al. (1979) found that Eueidaris graze heavily on live Pocillopora. In these areas fishes are not effective urchin predators, and urchins can limit the establishment and growth of coral reefs; reefs in these areas may have a maximum thickness that is only 12-25% of the thickness in areas where fishes prey heavily upon urchins (Glynn et al. 1979). Grazing by echinoids produces characteristic stellate dental browsing sculptures which can be preserved as trace fossils (Bromley 1975). Bromley (1978) suggests that some surface k grooves can be assigned to a particular species of echinoid and should be recognisable in geological cores. Echinoids both graze the coral and erode the coral surface to form a shallow depression, a "home cavity". To scrape away the coral substrate, they use their Aristotle's lantern, a complex of articulated plates surrounding the mouth, and perhaps their spines. To date there are no reports of dissolution of CaCO3 in the gut of echinoids. Presumably they are obtaining nutrients from the algae attached to the coral substrate or from the living coral tissue. Thus echinoids excrete similar sized particles of CaCO3 to those ingested. Grazing gastropods also contribute to surface erosion of coral reef substrates (Trudgill 1976) but are less important than either fish or echinoids. They tend to graze upon the epilithic, epi-endolithic and the shallow endolithic algae. They erode the surface coral substrates with their radulae which are made of calcite which is harder and denser than the typical aragonite or high magnesium calcite surfaces of the reef substrate. The large chiton Acanthopleura which feeds on the deeper endolithic algae, has the largest radula of the mollusc grazers studied by Trudgill (1976) and Lowenstam (1962) showed it to be made of teeth of magnetite with a hardness of about four and so the chiton is readily able to erode the coral reef limestones at Aldabra. Limpets may secrete an acid to excavate a home scar (Emery 1962); the conclusion was reached after recording pHs values of 5.~7.5 on the soles of the limpets. However, these results should be treated with some caution as the secretion of acid may be defensive (as described for other molluscs by Thompson 1960, 1961 and by Edrounds 1968). Taylor (1971) found the limpet Acmaea profunda down to 1.5 cm below the surface suggesting that limpets should be considered both as surface grazers and deep borers. The chiton Acanthopleura gemmata also uses its radula to excavate a "home site" and for grazing on the surface algae. Whilst grazing this chiton also removes a fine layer of limestone (Trudgill 1983 a). Thorne (1967) has shown that this species usually returns to its "home site" after feeding. Acid digestion of faeces, formed during the course of algal grazing, showed a weight loss of
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25-50%, indicating a significant proportion of carbonate ingestion and egestion during grazing (Trudgill 1983 a). The excretion of smaller sized particles of CaCO 3 than ingested was also indicated. Taylor (1971) has suggested that the gastropod grazers have adopted an optimal feeding-strategy whereby each species grazes to a different depth in the rock, and feeds on the algae associated with that strata. This reduces competition for food to a minimum.
b) Etching Three groups of organisms, the bacteria, fungi and algae, may use this means of penetrating coral substrates (Golubic et al. 1975). From laboratory experiments on crystals of calcite, Risk and MacGeachy (1978) have suggested that bacteria may be involved in the breakdown of limestone surfaces. They inoculated crystals of calcite with bacteria and found that the crystals developed etched surface and enhanced cleavage faces which would facilite breakdown of the crystals. However, far more work is needed to document the destructive role of bacteria in the field and if bacteria can also etch aragonite, of which coral skeletons are composed of, as well as calcite. The evidence for fungi boring into coral reef substrates is equally tenuous, although fungi are abundant in marine carbonates (Kohlmeyer 1969). Possible fungal filaments have been reported from an Upper Devonian coral (Kobluk and Risk 1974), where they occur in association with micrite tubercles presumably made by boring algae. No evidence of boring fungi has been found in the initial stages of bioerosion at Lizard Island, Great Barrier Reef. Kohlmeyer (unpublished data) examined coral blocks exposed during the study by Davies and Hutchings (1983). Microborings apparently made by fungi have been recognised within carbonate particles making up the surface sediments of the Arlington Reef Complex, Great Barrier Reef. Rooney and Perkins (1972) have suggested that fungi are one of the first endolithic organisms to attack skeletal debris. The boring properties of endolithic algae are, by comparison, well documented. For a review, see Golubic et al. (1975). Live endolithic algae are commonly visible as a greenish band just below the live coral tissue. Although commonly known as the "Ostreobium band", this feature may be made up of several genera of endoliths (Risk and MacGeachy 1978). The development of these highly pigmented algal bands occurs where and when conditions within the coral skeleton are optimal for vigorous growth, and Highsmith (1981) has suggested such conditions may be analogous to phytoplankton blooms where small populations expand rapidly when conditions such as light, temperature and nutrient concentrations co-occurs. Highsmith discusses the factors which determine the amount of light available to the algae, and the theories which may explain the presence of multiple algal bands
in some coral skeletons. The endolithic algae which belong to the Cyanophyta have special boring filaments about 5-10 ~tm wide. Algal penetration of coral skeletons generally follows planes of least resistance. Kobluk and Risk (1977 a, b) have investigated experimentally the rate and nature of infestation by endolithic algae by using an artificial non-marine substrate. Algal infestations occur rapidly after a clean substrate of Icelandic Spar crystals are exposed. Initially boring rates are very high but then decline. Boring initially is controlled by the orientation of the crystals but, with increased densities, boring becomes randomly orientated. With time, the algae advance downwards leaving behind a weakened heavily bored micritic rind. This micritic envelope is formed by repeated boring and infilling of borings by precipitated micrite (Bathurst 1966). Exposed filaments of algae may become calcified and this cementation will reduce permeability and porosity of the underlying substrate (Kobluk and Risk 1977 a, b). This process of algal infestation described by Risk and MacGeachy (1978), for non-marine substrates which they then suggest as the mechanism by which boring occurs in coral substrates must be treated with caution until the process is actually described for coral substrates. There is also some confusion in the literature as to what impact Ostreobium spp have on the coral skeletal structure. Kanwisher and Wainwright (1967) have measured the amount of damage caused by the algae, whereas Highsmith (1981) was unable to detect any macro-scale damage attributable to Ostreobium spp. Endolithic algae can be recognised in cores. Rooney and Perkins (1972) have used these characteristic algal bands to identify the depth at which these sediments occurred and have also used them as sediment tracers.
c) Infaunal borers 1. Sponges Boring sponges have probably received the most attention of all the groups of boring animals. Although the boring activity of sponges has been known for some time it was not until the late 1960's that their importance in processes of erosion, sediment production and calcium carbonate dissolution was realised (Neumann 1966; Wulff and Buss 1979). The only comprehensive taxonomic study of boring sponges has been made by R/itzler (1974) in Bermuda. He suggests strongly that the current distinction between burrowing and non burrowing families is artificial and that both habits may occur within a group of closely related species. Recently, extensive collections of boring sponges from the Great Barrier Reef have been made by Risk and Tudhope and several new species are being described. From these studies it appears that some boring sponges have a circumtropical distribution occurring on both Caribbean and Indo-Pacific reefs. However considerable work remains to be done on boring sponge taxonomy.
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Bromley (1978) attempted to characterise the burrows of individual species of sponge borers in present day reefs in the hope of being able to recognise these in the fossil record. A wide variety of cavities are created by sponges and, with the limited sponge fauna in Bermuda, Bromley was able to characterise the cavities created by each species. He suggests that the cavities should remain identifiable after fossilisation. Boring sponges form large chambers, with smaller galleries branching off the main chambers. Depth of penetration varies but usually does not exceed 20 mm (Wilkinson 1983). Although sponge borings are widely recognised in ancient reefs, individual species have not yet been recognised. This should be possible. Species resembling present day Demospongiae are recognisable from the early Cambrian (Finks 1970; Ziegler and Rietschel 1970). Wilkinson (1983) has discussed the alternate dominance of sponges and corals in calcareous reef structures during the Palaeozoic. Whether boring sponges in any way contributed to the alternating dominance is as yet unclear. Detailed studies on the processes involved in sponge boring have been carried out (Riitzler and Rieger 1973; Pomponi 1977, 1979). The sponge tissue has specialised etching areas responsible for the boring. The etching areas consist of etching bodies and numerous associated cell bodies. Etching commences at the periphery of the etching cell and as it proceeds a filopodial sheet of membrane-bound cell cytoplasm approximately 0.23 g thick extends into the substrate in a hemispherical fashion. Pomponi (1979) believes that the substrate is dissolved by a cellular lysosomal system dissolving any organic matter and by carbonic anhydrase regulation of acid secretion occurring at the periphery of the filopodial sheet. When the opposing filopodia meet, a chip of substrate is released which, together with the spent etching cell is transported through the sponge to an exhalent canal and expelled. Sponge boring results in about 98% of the bored substrate being disposed as chips. The remainder is dissolved. Sponge chips have a characteristic shape and morphology and can be recognised in sediments. The role of sponges in coral bioerosion and subsequent modification of reefal morphology has recently been discussed in detail by Wilkinson (1983), and previously by Goreau and Hartman (1963). 2. Bivale molluscs The habit of boring into rock, coral and shell is extremely well developed within three families of bivalves. The Pholadidae are exclusively borers using primarily mechanical means of penetration; the Gastrochaenidae and some species of Mytilidae penetrate predominantly calcareous substrates using mechanising which, in part, are chemical. Several other genera of boring bivalves belong to families that are not exclusively borers. For a taxonomic discussion of boring bivalves together with their burrow characteristics see Evans (1970) and Warme (1975). Indi-
vidual bivalves have such characteristically shaped burrows that they can be easily recognised in cores (Bromley 1978). The majority of studies on boring bivalves (Gardiner 1902, 1903 - Indian Ocean; Otter 1937; Kleeman 1980 Great Barrier Reef; see Yonge 1963 for a review) have been qualitative. The few figures available on densities suggest that 50-500 pholad bivalves /m 2 m a y occur (Warme 1975) but these figures fail to take into account their patchy distribution. Recently, Highsmith (1980) has obtained some figures of bivalve densities by examining coral heads in Museum collections. He found considerable variations in the densities and he was able to rank them as follows; eastern Pacific > western Atlantic > Indian Ocean > western Pacific. He postulates that these differences are highly correlated with global patterns of plankton primary productivity. However these studies should be confirmed by field observations as obviously there is considerable bias in selecting coral heads for Museum collections, and until these are carried out Highsmith's postulation must be regarded as tenuous. Loya (1982) has already questioned the validity of Highsmith's data for the Gulf of Eilat where he has recorded much higher densities in the field. Lithophagid bivalve molluscs, which belong to the F. Mytilidae, bore by chemical dissolution of the coral substrate. Ansell and Nair (1969), Warme and Marshall (1969) and Otter (1937) have shown that glands at the pallial edge of the mantle can be protruded and secrete an acid which causes dissolution and pre-softening of the rock. The actual removal of the pre-softened particles is achieved by a rocking movement of the shell. Soliman (1969) and Purchon (1968) have shown how the shell is adapted for mechanical boring with a thick protective coat of periostracum at the anterior boring end. The shell can move up and down and rotate within the burrow which causes the shell valves to rock about the vertical axis in order to accomplish the mechanical boring. It seems that the other groups of boring molluscs bore in a similar way to the lithophagids. 3 Sipunculans Sipunculans are prominent endolithic animals in many reef areas, boring into live and dead coral but also excavating hard, well cemented limestones both in the intertidal and subtidal (Warme 1975). The only detailed study of sipunculan distribution is by Rice and MacIntyre (1982) on the sipunculans of Carrie Bow Cay, off Belize in the Caribbean. Rice and MacIntyre recorded eight species of which six were borers in coral substrate. The greatest species diversity occurred on the reef crest, They found that several species may occur in the same coral rock suggesting that physical factors associated with locality, such as agitation and depth of water, may be even more significant than the structure of the coral skeleton in determining the specific distribution.
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Rice and MacIntyre stress though that these interpretations are tentative. Many other workers, (Kohn and Lloyd 1973; Peyrot-Clausade 1974; Hutchings 1974, 1978) have recognised the importance of sipunculans in boring communities but have not considered them in detail. Recent work by Davies and Hutchings (1983) has indicated that sipunculans are not initial colonisers of newly available coral substrate. However, within 2-3 years of coral substrate becoming available, they become abundant and many individuals exceed 2 cm in length (Hutchings 1983b; Hutchings and Bamber 1985; Kiene 1985). The mechanism by which sipunculans bore into coral substrate is largely speculative. Many boring sipunculan species possess a wide variety of hooks, spines, papillae or other structures embedded in their leathery skin. These structures probably anchor the worms in their domicile and function as tools for boring. They are deployed at the tip, base, along the length of the introvert, along the side of the body or at the posterior extremity (see Fig. 11-15 in Warme 1975). It is assumed that these structures enable the sipunculan to mechanically grind its burrow. Their borings are variable; most are simple, blind, straight to gently curved, or even highly sinuous tubes containing a single specimen (Rice 1969).
animal grows, it enlarges its burrow. Rates of boring seem rather slow and if an adult boring species is exposed, it has little chance of surviving long enough to bore another burrow before being predated upon. This will happen during storms as large heads of corals are dislodged and rolled about on the substrate. Recruitment of boring animals may be seasonal, exhibit considerable year to year variations and vary between different parts of the reef. Such variability has been documented in a wide variety of reefal organisms including boring polychaetes, that it probably represents the norm for all reefal organisms (Hutchings 1981, 1984; Hutchings and Murray 1982; Sale 1983; Wallace 1983). This variability in recruitment may have a considerable impact on the rates of bioerosion. The above discussion of the major agents of boring in coral substrates is not intended to be comprehensive (for references to major review articles on boring organisms see Table 11.1 in (Warme 1975). Rather, it has been used to illustrate the variety of organisms involved in boring and to provide a background for the remainder of the paper. Some minor agents of boring such as the zoanthids, barnacles and bryozoans have not been discussed, but see Warme (1975).
4. Polychaetes
Published rates of biological destruction of coral reefs illustrate how few detailed studies have been undertaken. Recently Trudgill (1983 a) has summarised much of the quantitative data available.
Most marine annelid worms are polychaetes, a very diverse group (Fauchald 1977). Several polychaete families have boring species and probably not all have yet been documented. The important boring species belong to the following families, Eunicidae, Lumbrineridae, Dorvilleidae, Spionidae, Cirratulidae and Sabellidae. The mechanism of boring in polychaetes is not well documented. Blake and Evans (1973) reviewed all the data on mechanisms of boring in the genus Polydora (F. Spionidae) and suggest that chemical dissolution of the coral substrate was most likely. Subsequently, Zottoli and Carriker (1974) investigated boring in Polydora websteri, which bores into the shell of oysters and mussels. The worm secretes a viscous fluid which dissolves the organic matrices of the molluscan shell, and produces shell fragments which are incorporated into the mud lined tube of Polydora. Perhaps a similar mechanism operates in coral boring species of Polydora. Boring by chemical dissolution is also the most likely method in the cirratulids and sabellids. However the eunicids, lumbrinerids and dorvilleids may bore by mechanically grinding the substrate with their well developed sets of teeth.
Recruitment of boring animals Probably all infaunal borers are recruited to coral substrates by pelagic larvae (McCloskey 1970), so that larvae or newly metamorphosed individuals must have a capacity for rapid penetration of the coral substrate. As the
II. Rates of biologic destruction of coral reefs
a) Grazers Rates of bioerosion caused by parrotfish have been estimated in the Caribbean to be between 4 0 4 9 0 g m - ~y- 1 (Gygi 1975; Ogden 1977; Frydl and Steam 1978). Sediment turnover in lagoons which further reduces particle size, by scarids and other browsers and grazers has been reported, as resulting in a loss ranging from 40-980 g m - 2 y -~ (Cloud 1959; Bardach 1961; Gygi 1975; Ogden 1977; Frydl and Steam 1978). At Lizard Island, Great Barrier Reef, parrotfish activity varies according to the nature of the environment. There, heaviest parrotfish grazing occurs on lagoonal patch reefs (Kiene 1985). These observations coincide well with the recently published data of Russ (1984a, b). He has studied the distribution of herbivorous grazing fish in the central Great Barrier Reef, and found (Acanthuridae, Scaridae and Siganidae) that recognisable patterns of distribution occur across the shelf. Maximum densities occur on mid and outer shelf reefs and minimum numbers on the inshore reefs. Within a reef distinctive asembtages of fish could be recognised according to the habitat. Russ found that species which feed by cropping and scraping the algae were more abundant in shallow zones (reef crest, reef fiat and lagoon) than in deep zones (reef slope, back reef) and hence rates of grazing and bioerosion should be higher in the shallow zones of the mid and offshore reefs. However
244 Choat (1983) suggests that grazing by scarids is a highly complex and variable process, and that feeding rates obtained from a limited data base should be treated with caution. Choat working at Lizard Island also found that densities of scarids could be correlated with habitat and depth, but this was not necessarily correlated with observed feeding rates. Thus it may be inaccurate to assume that high densities of scarids in a particular environment will lead to high levels of feeding and consequently bioerosion in that environment. Estimates of rates of bioerosion attributable to echinoids are restricted to Caribbean and Eastern Pacific reefs. On Barbados fringing reefs, echinoids are responsible for the removal of about 9 kg m-2y -1 of CaCO 3 which is equivalent to a surface erosion rate of 6 mm y - 1 (Hunter 1977; Stearn and Scoffin 1977). Eucidaris which occurs in densities of 10-50 individuals per m 2 in Galapagos removes about 1.2 kg m - ly- 1 of CaCO 3. In areas of high coral cover (60-80%), this loss represents about 10-20% of the total CaCO 3 produced by the reef. Along the reef crest where coral cover is low (30%) and where maximum concentrations of the echinoid occur, no net gain of CaCO3 occurs. Under such conditions echinoids not only cause significant bioerosion at the present time but essentially prevent reef growth (Glyn et al. 1979). Hunter (1977) has suggested that the sea urchin Diadema antillarum produces significant amounts of sediment from the coralline algae, on which it feeds, on a Barbados fringing reef. Hunter suggests that this echinoid is the major sediment producer on Barbados reefs. Trudgill (1976) has measured the rates of grazing of the chiton, Acanthopleura, in a variety of habitats at Aldabra, Indian Ocean, and has found rates varying between 0.45 mm y - 1 to 0.61 mm y - 1. Higher rates of loss between 0.2-3.8 mm y-~ have been reported from One Tree Island, Great Barrier Reef (Trudgill 1983b). This loss consisted of two components, the loss of CaCO 3 by home scar excavations measured as 0.2-2.9 mm y- 1, and 0.1-3.0 g m - 2 day- 1 during grazing, ingestion and egestion. This is equivalent to 0.02-0.7 mm y-1. McLean (1974), working at nearby Heron Island, reported figures which fall within the range quoted by Trudgill (1983 b). In the same study, Trudgill measured the surface lowering rates around Saccostrea pedestals, and they ranged from 0.2-3.8 mm y- 1 with a mean of 2.04 mm y- 1. These data also can be compared with the rates of 1.0-1.5 mm y-1 calculated by Hedley (1906) on nearby Masthead Island and they fall within the range of 0.54.0 mm y-1 quoted by Trudgill (1976) for Aldabra Atoll. However extrapolation of rates from a few observations may be tenuous (McLean 1967). Many factors determine the rates, including size of animal, hardness and mineralogical composition of the substrate, depth of penetration of the algae on which gastropods are feeding, and finally the life cycles and habits of the individual species. These factors should be borne in mind when extrapolating rates of any destructive or erosional agent from a restricted area to an entire reef. Finally it should be stressed that all the
measurements of rates of loss of CaCO3 given above have been extrapolated from rates determined from small experimental study sites on the assumption that these rates are typical for the entire reef, which is obviously not true. But the figures do give an indication of the severe, localized impact, grazers can have on both coral and coral reef substrates. No rates of etching are available for any reefal environment.
b) Infaunal borers Estimates of the importance of sponge boring vary considerably. MacGeachy (1977) estimates that sponges account for 90% or more of the total boring in most coral heads examined on some Barbados reefs. In Florida, Hudson (1977) showed that sponge erosion is capable of reducing a 1 m high Montastrea annularis head at the rate of 14-67 mm y - 1 which is equivalent to a loss of 3.013.4kg CaCO3 m - 2 y -1, according to extrapolations made by Davies (1983). Using these rates, this would mean that a completely solid 1 m high colony ofM. annularis would be reduced to sediment in 150 years. Hudson suggests that the time would in fact be less, as live colonies have already been considerably bored at their base while still alive. Much higher rates were obtained experimentally by Neumann (1966). Extrapolating from these figures he calculated that 22-23 kg CaCO 3 per m -2 of sponge per y-1 could be produced as sediment by sponges. Sponge chips comprise 30% of the total lagoonal sediment at Fanning Atoll (Ffitterer 1974) and 40% of silt sized sediments within patch reefs off Belize (Halley et al. 1977). Rates of bioerosion on three massive corals on the Belize barrier reef have also been measured by Highsmith et al. (1983). They found significant differences in rates between the 3 species of coral, but in all cases boring sponges accounted for 85-94% of the skeletal excavation. Rates varied according to skeletal density (dense species are more bored) and the proportion of dead skeletal surface available for recruitment by boring organisms. They did not provide the actual data so that the amount of CaCO3 removed per unit time could not be calculated from their published data. Some of the rates for sponge boring have been calculated on the basis that the rate of boring is constant over time. So if the total amount of CaCO3 removed is calculated for a coral colony of known age, the rate of bioerosion per year can be determined (MacGeachy 1977). However this assumption that sponges bore at a constant rate has not been substantiated by Rfitzler's (1975) experimental work. He monitored the rates of sponge boring and found that rates are high initially as the sponge penetrates the substrates resulting from mechanical stimulation and lack of competition. Rfitzler does not explain exactly what is meant by mechanical stimulation, but it may refer to development of a minimum sized sponge colony as rapidly as possible after the initial penetration of the sponge larvae.
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Once the colony has reached a critical minimum size, growth rates slow up. This concept of mechanical stimulation has also been raised by Neumann (1966). Grazing of the sponge colony may also stimulate boring rates. Within 6 months the rate drops and the optimal long term erosion of CaCO3 does not exceed 700 mg m - 2y- 1, at least for the two species of Cliona studied. Substrate limitations and competition for space and food will further reduce this rate. Several other factors may affect growth rates, such as light levels, currents, and temperature. Rfitzler found that strong water movements stimulates the rate of boring. Preliminary observations on the reproductive cycle of Cliona lampa, a common Carribean boring sponge indicate that the peak of reproduction coincides with the cooling of seawater, so that a peak of recruitment of boring sponges should occur in late autumn, and subsequently increased rates of boring at this time, until the colonies have become established. This agrees well with the observed patterns of sponge boring, that they often do not penetrate into the calcareous substrate further than 1-2 cm. Extrapolating from his data and from field observation. Riitzler suggested that on the platform reef at Bermuda, the burrowing potential of sponges is about 256 g CaCO3 m - 2 substrate y-1, which is a much lower figure than those calculated by Neumann (1966), (based on an average abundance of sponges on the reef platform of 16 g dry weight of sponge per m2), Hudson (1977) and MacGeachy (1977) but perhaps a more realistic figure as it incorporates fluctuations in boring rates with time. Rtitzler (1975) calculated that 97-98% of the sponge eroded limestone remains in particulate form on platform reefs. In these areas, up to 250 g m - 2 y - 1 of fine sediments consisting of coral chips produced by sponge boring could be generated. The variations in rates obtained experimentally by several workers (Neumann 1966; Riitzler 1975; Bak 1976) suggest that rates may vary according to species of sponge, substrate and to the environment. There is some evidence that boring sponges tend to favour colonising existing pores such as those made by endolithic algae (McCloskey 1970). The amount of damage done by a sponge to a coral skeleton will be largely determined by the porosity of the coral species. More material is removed from massive corals with less porous skeletons than from less massive more porous species (Buddemeier et al. 1974). Thus many factors need to be taken into account when extrapolating general rates of sponge boring, from a single species of sponge boring into one particular species of coral. Recent work on the Great Barrier Reef by Davies and Hutchings (1983) has shown that sponges play no part in the initial bioerosion of newly available coral substrates, at least in the three environments investigated, viz. the reef slope, reef flat and a lagoonal patch reef at Lizard Island. Subsequent studies by Hutchings (1983a, b and
1985), and Kiene (1985), have shown that boring sponges begin to enter the substrate after 2-3 years. Few figures are available for boring rates attributable to polychaetes. Polychaetes are the initial colonisers of newly available coral substrates and distinct successional phases in the development of these communities occur. Davies and Hutchings (1983) recorded rates varying from 0.6-1.7 kg CaCO3 m-2y - J at Lizard Island, Great Barrier Reef and subsequent work by Hutchings and Bamber (1985) in a greater variety of reefal environments at Lizard Island, found rates of 0.33-4.816 kg m-2y - 1, attributable only to polychaetes. These rates will vary according to substrate and environment as do densities and species composition of boring polychaetes (Hutchings 1974; Hutchings and Weate 1977, 1979). Superimposed upon this will be seasonal and inter-year variations in recruitment of polychaetes and hence numbers of infaunal polychaetes (Hutchings 1981, 1983 a, b, 1985; Hutchings and Murray 1982). Few estimates of CaCO3 loss attributable to bivalves are available. On the Great Barrier Reef, Hamner and Jones (1976) estimated erosion by Tridacna crocea at 014 kg CaCO 3 m-2y -~. In some areas of the Great Barrier Reef, much higher densities of a related species Tridacna maxima occur. McMichael (1974) estimated a population of 2 million at One Tree Island. However, T. maxima does not bore as extensively as T. crocea which is normally completely embedded in the reef substrate, whereas T. maxima is often found occurring completely detached from the substrate. The impact of this biological erosion on the original substrate was not commented upon but it must have been considerable (McMichael 1974). Giant clams are recognisable in early Holocene reefs and if similar densities occurred to those on recent reefs, giant clams have had a considerable ongoing impact on reef morphology. Trudgill (1976) reported the boring rate of Lithophaga as 0.911 cm y- 1 and Lithotryra as 0.844 cm y - 1 at Aldabra, Indian Ocean. The boring rate increases with age up to 5-6 years of age. After this, the rate varies widely, coinciding with a growth plateau of the molluscs as the individuals become mature and subsequently senescent. More detailed studies of this kind are needed elsewhere to assess the importance of boring bivalves. Also, information is needed about the factors important in determining the distribution and abundance of boring bivalves. This will necessitate studying recruitment patterns, variations of boring rates between different sized individuals and variations between substrates and environments. Trudgill (1976) emphasises that variations in exposure of the environment, substrate hardness and competition from other species may cause variations in rates of bioerosion. III. Factors in determining rates of bioerosion
Until recently, studies have calculated rates ofbioerosion for a particular group of animals, and assumed that they
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are constant over time and often within a range of different habitats on the same reef. I should like to suggest that this is unlikely for several reasons, and that the few quantitative estimates on rates of bioerosion should be treated with caution. The prime role of these estimates should be to stimulate long-term detailed studies ofbioerosion both within and between reefs. The reasons for suggesting that rates of bioerosion are not constant over time or between reefs are several. The first of these is the variability across the reef in larval recruitment of some of the agents of bioerosion (Hutchings 1981, 1984, 1985; Hutchings and Bamber 1985). Hutchings and Murray (1982) have shown that some species of polychaete exhibit strong seasonality of recruitment and many species, including boring species, exhibit marked inter-year variations in recruitment success. Subsequent analysis of more long-term data on polychaete recruitment (Hutchings 1984, 1985) has further demonstrated the unpredictability of polychaete recruitment. Other reefal organisms which have been investigated in detail, such as corals and fish, exhibit similar annual and seasonal variations in recruitment (Sale 1980, 1983; Sammarco 1983, Wallace 1983). I would therefore predict that the other boring organisms such as sponges, sipunculans and bivalves would exhibit annual and seasonal variations in recruitment success. Riitzler (1975) has suggested that at least one species of boring sponge in the Caribbean spawns in late autumn. No other information on spawning times of boring sponges seems available. I would further suggest that this pattern of unpredictability may be the norm for most reefal organisms. The larvae of boring organisms may be fairly selective as to the orientation of the surfaces into which they bore (Risk and MacGeachy 1978) and some unpublished data of Hutchings suggest that many species select vertical surfaces for settlement and subsequent boring. So that the orientation of available substrate may be an important factor in determining rates of bioerosion (Hein and Risk 1975). Thirdly, coral reef substrates do not become heavily bored until the veneer of living coral tissue dies (McCloskey 1970). This death may occur at any time of the year as the result of natural mortality, predation or physical destruction. Perhaps, after a plague of Acanthaster planci where virtually all the coral is killed, rates of bioerosion may increase though this has not been investigated. The suite of larvae available for recruitment will be determined by the time of year and which year the substrate becomes available (Hutchings 1981, 1984; Hutchings and Bamber 1985). Such variability may be caused by variations in water movements around a reef (Frith et al. in press). The rate at which the substrate becomes colonised by borers will also be affected by the time of year when the substrate becomes available. Substrates being released in mid winter have low rates of colonisation until the following spring when rapid recruitment occurs. On the other hand, if the substrate becomes available in the spring, recruitment is initially very
rapid and then tapers off during the following winter (Hutchings 1983a; Kiene 1985). Distinct succession occurs in the boring community (McCloskey 1970) and it appears that these successional changes are characteristic of a particular environment. For example, within the polychaetes, cirratulids are the initial colonisers, and are replaced by either sabellids or spionids depending upon the reefal environment at Lizard Island (Davies and Hutchings 1983). Whether these differences in the communities related to site effects are retained subsequently is not yet known, however, after 21/2 years, particular sites still have characteristic faunas. Windward sites have a more diverse boring fauna than leeward sites. Detailed polychaete succession has yet to be documented in other geographical areas. Several other workers have noted variations in boring communities across a reef. Warme (1975), working in Jamaica, found that habitats in sheltered bays have a more diverse fauna than similar sites on the open reef and foreshore reefs, the reverse of the situation found at Lizard Island. Cloud (1959) found more sipunculans in the lagoon at Saipan than offshore. Obviously the distribution of corals varies across the reef, and hence the types of coral skeleton available for boring (Done 1982). Recently, Crossland (1982), working in Abrolhos Islands off the north west coast of Australia, has found that the density of coral skeleton is significantly less than for the same species occurring on the Great Barrier Reef. Hutchings (personal observation) found dense cryptofaunal communities in dead coral substrate collected at Abrolhos and it appears that the biomass of eroders is much higher than on the Great Barrier Reef. However no figures are available for rates of bioerosion in the Abrolhos. Another factor which should be considered is the stage of development of the reef (Davies 1983). Intuitively one would expect to find considerable differences in both rates and causal agents in reefs at varying stages of development. A study to investigate this is just beginning in the Capricorn Bunker Group of the Great Barrier Reef (Kelleher 1983). Boring communities are not stable over time. Individuals are replaced and probably many generations of borer occur within the time span of a boring community, and the components of the boring communities also change with time. These changes in the composition of the boring community may modify rates of bioerosion. Risk and MacGeachy (1978) have suggested the following succession of bioeroders; bacteria, followed by algae and fungi, then clionid sponges and fungi, followed by clionid sponges and spionid polychaetes, then other sponges and eunicid polychaetes, and finally mytilid bivalves, barnacles and sipunculans. This boring activity results in up to 70% of some coral heads being destroyed, with consequent weakening of the reef structure and production of large volumes of sediment. This is the pattern Risk and MacGeachy found in the Caribbean. Choi (1984) has also documented a similar succession in the
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Caribbean. The initial pattern, at least, is apparently different at Lizard Island, Great Barrier Reef (Davies and Hutchings 1983) where polychaetes are the initial borers, with bivalve molluscs and sipunculans gradually entering the community 12-15 months later. Subsequent work by Hutchings and Bamber (1985) has shown that despite larval sipunculans and sponges being available for recruitment, newly laid coral substrates are not bored by these organisms until 9-12 months of polychaete boring has occurred. This suggests that polychaetes in some way modify the coral substrate making it more attractive to other types of boring organisms. Variations in rates of boring within the lifespan of an animal have only been investigated for sponges, where the rate is initially high as the colony establishes itself but then the rate falls (Neuman 1966; Riitzler 1975). Similar patterns are probably exhibited by other borers especially the longer lived species which are probably sipunculans, bivalve molluscs, and some of the larger polychaetes such as the eunicids. Most .of these animals grow rapidly initially, but subsequently growth rates taper off, and as these borers live in custom fitting burrows, it follows that boring rates will decline with growth rates of the organism. Superimposed on all these factors are seasonal growth patterns of the boring agents, which may be determined by the seasonality of food supply etc. Even tropical coral reefs have distinct seasonality. Lizard Island (Lat. 14~ has at the surface and at 10 m depth an annual water temperature range of 8 ~ in the lagoon and over the fringing reefs and reef flats (CSIRO unpublished data, collected over 5 years). Currently little information is available on the variations in the rates of bioerosion of a community over time but studies are currently underway at Lizard Island, Great Barrier Reef to investigate this (Hutchings and Bamber 1985; Kiene 1985). Strong currents may influence the rate of solution of substrate and the removal of eroded sediment or alternatively it may force sediment or alternatively it may force sediment into eroded substrates and encourage cementation and reduce the net rate of bioerosion. Trudgill (1976) working on the marine limestone shores of Aldabra, Indian Ocean, found that on sheltered coasts the boring rates are far greater than those for surface erosion, whereas on exposed coasts the rates for surface retreat by chemical and physical erosion may approach those of boring. From the few data available, it is difficult to discuss geographical variation in rates of bioerosion. However data from Highsmith (1980) on boring bivalves suggest marked geographical variations. Echinoids which are a major agent of erosion in the Caribbean (Sammarco 1980, 1982) are, by comparison, almost absent on the Great Barrier Reef. The recent findings of Hay (1984) however, strongly imply that the densities of echinoids found by Sammarco on Jamaican reefs are typical only of heavily overfished reefs. So probably the role of echi-
noid grazing in typical reef should be reassessed. Echinoids are present on the Great Barrier Reef but are primarily cryptic and nocturnal, (Hutchings personal observation at Lizard Island) but whether these relatively small populations have an impact on bioerosion by grazing remains to be investigated. Apparently boring sponges may also be more important in the Caribbean than on the Great Barrier Reef (Hein and Risk 1975; Rfitzler 1975). The reasons for these variations are not clear but may reflect the geological history of the reef. If boring communities are environment specific and produce characteristic bores, these should be recognisable in geological cores and facilitate the recognition of particular environments. Many of the present day borers are clearly recognisable in ancient reefs, so boring communities have long been characteristic of coral reefs (Bromley 1978). Whether the species composition and or the relative proportions of the major borers present, was similar to those present in recent reefs has not been evaluated. Comprehensive descriptions of boring communities are needed in both ancient and modern reefs in order to understand the long term significance of boring on reefs. Organisms capable of destroying calcium carbonat substrates have an extensive fossil record. The oldest known reef macroborers have been found in the Lower Cambrian Forteau Formation in southern Labrador (James et al. 1977). These macroborers are known only from their vacated boreholes, which closely resemble the burrows made in modern reefs by sipunculan worms. From the middle Cambrian to the Middle Ordovician, only one genus of macroborers is known, plus several reports of endolithic algae and fungi. This low diversity of macroborers is presumed to be due to a lack of suitable skeletal substrates. With the rise of complex organic reefs in the middle Ordovician, macroborers began to radiate and diversify. The co-existence of reefs and bioeroding organisms is evidently a relationship which has lasted at least 550 million years (Risk and MacGeachy 1978).
IV. Consequences of biological destruction on coral reefs
The impact of bioerosion on coral reefs is complex. Bioerosion creates a large number of reef habitats, each characterised by its own community, which are integral parts of a coral reef, one of the richest and diverse marine ecosystem known (Connell 1978). Together with physical erosion, bioerosion is responsible for the creation of newly available substrates as weakened coral colonies become dislodged during storms. This newly available substrate is then colonised by sedentary species including corals (Sammarco 1980, 1982). These small scale disturbances have been postulated as being important in maintaining the species diversity of reefs (Connell 1978).
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Bioerosion creates additional burrows for colonisation by non-boring species and this cryptofaunal community (Hutchings 1983 b) may play a major role in the recycling of nutrients on the reef. Many of the species are deposit feeders and draw down into the coral substrate the sheets of mucus produced by the corals together with any trapped particles. The cryptofauna is in turn eaten by a wide variety of molluscs and fish (Kohn and Nybakken 1975; Vivien and Peyrot-Clausade 1974). Bioerosion will often increase the surface complexity of the coral substrate and hence increase the available surface for colonisation by a wide variety of animals. These non-boring animals may be important in modifying rates of bioerosion. The biological interactions which take place within the cryptofaunal community (i.e. borers and non-borers and interactions between boring species) have not been investigated. Sipunculan burrows often exhibit sharp angles as if they have been avoiding a nearby burrow (Rice 1969). But boring species must maintain an opening to the outside for feeding, respiration, breeding, etc and prevent encrusting species from overgrowing the entrance to their burrows. A well established infauna and encrusting fauna may modify the number and species of larvae able to settle and penetrate the coral substrate, and perhaps subsequently modify rates of bioerosion. Extensive grazing on live coral by parrotfish which has been observed at Lizard Island Great Barrier Reef, (Hutchings personal observation) may facilitate the settlement and subsequent boring by some animals and the recruitment of the serpulid worm Spirobranchus giganteus. As the removal of live coral polyps may provide a substrate on which larvae can settle and bore into the substrate without being predated upon by the coral polyps. However many activities of bioeroders actually encourage and facilitate reef growth. Several examples of this apparent paradox occur. In Hawaii, Brock (1979) has shown that coral and coralline algal recruitment is more successful in areas subjected to heavy grazing pressure by parrotfish than in areas of low fish grazing. Ogden and Lobel (1978) suggest that fish grazers may reduce the abundance of certain competively superior algae, thus allowing corals and cementing algae to survive. Similarly Sammarco (1980, 1982) has shown that high concentrations of the echinoid Echinometra viridis in the Caribbean create a situation in which growth and fusion of Agaricia spat are optimised. Fusion allows a young coral colony to attain a large enough size to survive damage incurred from grazing or from competitive overgrowth. Another echinoid Diadema antillarum, at lower densities increase the rate of survival, competitive success and growth of coral spat. Sammarco (1980) suggests limited grazing of algae creates the necessary space for successful coral settlement. At higher levels of grazing, recruitment of coral spat is low. Recently Risk and Sammarco (1982) have shown that corals inside damselfish territories are significantly more bioeroded than corals outside such territories. Most of
the destruction was caused by boring sponges (Cliona sp.) and sipunculans (Cleosiphon sp.). They postulate that increased bioerosion in the territories may be the result of one or more of the following (1) increased success of larval settlement, (2) reduced grazing and predation on macroborers and (3) increased food supplies for the borers due to the algal turf, which the defending fish prevent being grazed by herbivorous fish. Bioerosion may facilitate cementation. Many boring species create fine sediment which may be trapped within the burrows and subsequently this may become cemented. Boring algal filaments subsequently undergo cementation (Davies and Hutchings 1983). The infauna, both boring and non boring species, may bring sediment into the substrate for feeding and this may become trapped and subsequently cemented within the substrate (Marshall 1983). Ginsburg (1983) working in the Caribbean has shown the impact of bioeroders in producing a honeycomb structure which traps sediment as it is washed over the reef during storms, and subsequently this sediment may become cemented. Recently Choi (1982) has suggested that the entire infaunal community, including both borers and nestlers (Hutchings 1983 a) can serve as sensitive indicators of environmental stress. Thus, perhaps in the future, geologic cores through infaunal communities can provide information on environmental conditions operating at that time. V. The long term significance of bioerosion on coral reefs
From the relatively few quantitative estimates of rates, it would appear that bioerosion is a major component of the total erosional modification of reefs. Together with chemical and physical erosion it facilitates the formation of characteristic reef structures such as boulder tracts, eroded reef flats, cay and lagoonal sediments. Thus bioerosion is a major force in determing modern reefs morphology. Geological evidence suggests that agents of bioerosion are very visible in ancient reefs, suggesting that bioerosion has always been a major force in determining the shape and form of reefs. So far in this review, bioerosion has been considered as a discrete process. This is not strictly true. Rather, bioerosion is one of several forces acting on coral reefs simultaneously. These forces interact with each other at varying rates over biological and geological time scales. The major forces acting on coral reefs include growth and accretion by epibiotic and encrusting species, biological and physical erosion, cementation, and major physical determinants such as changes in sea level and sea temperature and subsidence. The variations of these forces over time are still controversial but some data are available and provide a useful framework for future studies. Growth rates of coral reefs are not constant either within a reef, over time or between geographical regions. Davies (1983) tabulates the available estimates
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of reef growth, on a world wide basis. They range from 0.38-12m 10-3yrs. Data from the Great Barrier Reef suggests that growth rate variations in the Holocene approximate a sine curve with slow rates of growth during reef initiation and again when the reef reaches the surf environment (Chappell 1983; Chappell et al. 1983). High rates of growth may occur during periods of rising sea level or subsidence (Scoffin 1977). These rates are calculated by radio carbon dating of cores. Such increases of growth rate could be obtained in a variety of ways including constant growth but reduced rates of erosion, increased growth with reduced or constant levels of erosion. No data are available as to whether significant changes in erosion rates occurred during the Holocene. Growth rates across a reef in Holocene reefs, however, have been shown not to be constant in time (Davies 1983; Davies and Marshall 1979, in press). Davies provides estimated rates of growth for the windward margin, the windward reef flat and the leeward reef flat on One Tree Island, southern Great Barrier Reef. Large variations occur both within and between these environments. However areas of active reef growth where high coral cover occurs such as reef fronts are not characterised by rapid rates of erosion. Davies and Hutchings (1983) found maximum rates of erosion, at least of initial erosion, on the reef flat where moderate rates of calcification occur (Kinsey 1983; Smith 1973). High potential growth rates, resulting from high calcification rates in windward reef environments, are modified by high destruction rates which act with hydrodynamic conditions to transport growth material to leeward sites of accrual. This conclusion supports a model of windward slopes dominated by erosion, while growth and expansion takes place in leeward environments (Davies 1983). During the evolution of a reef, areas of dominant reef growth may gradually evolve to areas of low growth and high rates of erosion (Davies 1983). Obviously more information is needed to fully document oscillations between rapid growth and rapid destruction. These data can only be obtained from present reefs by measuring rates of growth and erosion in a wide variety of habitats on reefs at different stages of evolutionary development (Davies 1983). Thus, rates of bioerosion may provide a sensitive indicator as to the stage of development a particular reef has reached. The highest levels of productivity occur on the windward margins (Kinsey and Davies 1979; Kinsey 1983). An important role of bioerosion on the windward slopes is to destroy the substrate and facilitate the transport of sediment and associated nutrients, to the leeward reefs, where levels of productivity are much lower. Bioeroders are constantly destroying the framework of a reef. If bioerosion consistently exceeds reef growth, then the reef framework and hence the reef will be destroyed (Ginsburg 1983; Stearn and Scoffin 1977). Bioerosion affects the porosity and permeability of the reef, which fa-
cilitates additional erosion by physical and chemical forces. However, it also may facilitate the trapping and subsequent cementation of sediment within the reef (Davies and Marshall in press). The majority of reefs are composed mainly of sedimentary facies rather than a coral framework. Recently, Davies and Hopley (1983) analysed cores from a large number of reefs along the Great Barrier Reef in terms of five Holocene bio-lithofacies: coralline facies, branchingcoral facies, coral-head facies, detrital carbonate facies and terrigenous facies. Detrital facies dominate the growth fabric of most reefs in the central Great Barrier Reef, in contrast to the northern and southern areas. Further examination of the detrital facies within the central area, reveals that they are dominant in the mid-shelf and fringing reefs of this area and constitute minor facies of the outer-shelf reefs. Davies and Hopley (1983) suggest that the inner shelf reefs are really detrital piles with coral caps. Thus there is not a latitudinal variation in reef structure but rather a west to east variation across the central shelf perhaps related to wave energy. A similar pattern is also seen in parts of the northern Great Barrier Reef. Davies and Hopley do not speculate on the origin of the detritus making up the facies only describing its distribution. One potential source of the detritus is bioerosion, and it could be produced inside or transported from outer shelf reefs to the mid and inner shelf reefs. To date no studies have been carried out on the transport of sediments, if any, across the Great Barrier Reef Province. Marshall and Davies (1982) have compared actual reef growth in terms of amounts of CaCO 3 laid down by coral skeletons with the actual, in place reef framework at One Tree Island, and found that the production of sedimentary facies is far more important than actual coral reef growth in maintaining the reef. Bioerosion is also extremely important in producing sediments which subsequently are not incorporated into the reef framework. A considerable proportion of the reef ecosystem consist of sediment communities and within the Great Barrier Reef Province, reefs constitute a small percentage of the total area. Recent work by Torgensen et al. (1983), working in Princess Charlotte Bay in North Queensland, has shown that 95% of the organic carbon in the sediment has a reefal origin, and that terrestrially derived sediments are limited to very near the shore line. They do not postulate the origin of this reefal sediment, but it may be the product of bioerosion. Recently it has been shown that marine invertebrates preserve in their calcareous skeletons, an isotopic and trace element record of the chemistry of the water in which they grew. Thus, boring animals such as molluscs preserved in cores will provide us with alternative ways of obtaining detailed information of the environment in which they lived (Aharon et al. 1980; Aharon and Chappell 1983). Finally, bioerosion as already suggested, may be very important in maintaining the high diversity of coral reefs
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by small scale local disturbances (Connell 1978). This will be extremely important in areas where physical disturbance is low, such as on protected leeward reefs. Bioerosion is therefore a very important agent determining the shape and form of coral reefs, although to date a very neglected one. Hopefully this review will stimulate some long term comprehensive studies to be undertaken on bioerosion. Only then can the real significance of bioerosion be assessed, for many of the points raised are at this stage speculative. These studies must include both the biological and geological disciplines, as bioerosion is a continuing process which has been affecting reefs since their inception. Acknowledgements. I should like to thank Peter Davies for suggesting the topic of this review, and for providing comments on the review throughout its long gestation. Don Kinsey also commented on a earlier draft. Much of the work in progress by the author is funded by MST.
References A~ Hussaini AH (1945) The anatomy and histology of the alimentary tract of the coral feeding fish, Scarus sordidus Klunz. Bull Inst Egypte 27:349-377 Aharon P, Chappell J (1983) Carbon and oxygen isotope probes of reef environment histories. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 1-15 Aharon P, Chappell J, Compston W (1980) Stable isotope and sea-level data from New Guinea supports Antarctic icesurge theory of ice ages. Nature 283:649-651 Ansell AD, Nair BN (1969) A comparative study of bivalves which bore mainly by mechanical means. Am Zool 9:857-868 Bak RPM (1976) The growth of coral colonies and the importance of crustose coralline algae and burrowing sponges in relation with Carbonate accumulation. Neth J Sea Res 10:285-337 Bak RPM (1985) Recruitment patterns and mass mortalities in the sea urchin Diadema antillarum. Proc 5th Int Coral Reef Syrup 5:267-272 Bak PPM, Carpay MEJ, De Ruyter van Steveninck ED (1984) Densities of the sea urchin Diadema antillarum before and after mass mortalities on the coral reefs of Curacao. Mar Ecol Progr Ser 17:105-J08 Bardach JE (1961) Transport of calcareous fragments by reef fish. Science 133:98-99 Bathurst RGC (1966) Boring algae, micrite envelopes, and lithification of molluscan biosparites. Lpool Manchr Geol J 5:15-32 Blake JA, Evans JW (1973) Polydora and related genera as borer in mollusk shells and other calcareous substrates. Veliger 15:235-250 Brock RE (1979) An experimental study on the effect of grazing by parrotfishes and role of refuges in benthic community structure. Mar Biol 51:381-388 Bromley RG (1975) Comparative analysis of fossil and recent echinoid bioerosion. Palaeontology 18:725-739 Bromley RG (1978) Bioerosion of Bermuda reefs. Palaeogeogr Palaeoclimatol Palaeoccol 23:169-197 Buddemeier RW, Maragos JE, Knutson DW (1974) Radiographic studies of reef coral exoskeletons: rates and patterns of coral growth. J Exp Mar Biol Ecol 14"179-200 Chappell J (1983) Sea-level changes and coral reef growth. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 46-55 Chappell J, Chivas A, Wallensky E, Polach HA, Aharon P (1983) Holoeene Palaeo-environmental changes, central to northern Great Barier Reef inner zone. BMR J Aust Geol Geophys 8:223-235 Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302-1310 Choat JH (1966) Parrot fish. Aust Nat Hist 15:265-268
Choat JH (1983) Estimation of the abundances of herbivorous fishes and their grazing rates within reef systems. In: Baker JT, Carter RM, Sammarco PW, Stark KP (eds) Proceedings of the Inauguree Conference, Townsville Great Barrier Reef 1983. JCU, Townsville pp 171-177 Choi DR (1982) Coelobites (reef cavity dwellers) as indicators of environmental effects caused by offshore drilling. Bull Mar Sei 32:880-889 Choi DR (1984) Ecological succession of reef cavity dwellers (Coelobites) in coral rubble. BUll Mar sci 35:72-80 Cloud PE (1959) Geology of Saipan, Mariana Islands. Part 4: Submarine topography and shoalwater ecology. US Geol Surv Prof Paps 280-K K361-K445 Crossland DJ (1982) Seasonal growth of Acropora of formosa and Poeillopora damicornis on a high latitude reef (Houtman Abrolhos Western Australia). Proc 4th Coral Reef Syrup 1:663-668 Darwin CR (1845) Journal of researches during the voyage of H.M.S. Beagle. Nelson, London (Reprint) Davies PJ (1983) Reef growth. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science Townsville, pp 69106 Davies PJ, Hopley D (1983) Growth facies and growth rates of Holocene reefs in the Great Barrier Reef. BMR J Aust Geol Geophys 8:237-251 Davies PJ, Hutchings PA (1983) Initial colonization, erosion and accretion on coral substrate: experimental results. Lizard Island Great Barrier Reef. Coral Reefs 2:27-35 Davies P J, Marshall JF (1979) Aspects of Holocene reef growth - substrate age and accretion rate. Search 10:276-279 Davies PJ, Marshall JF (in press) Age and uthologic structure of holocene reefs in the southern Great Barrier Reef. Coral Reefs Done T (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95-108 Edmunds M (1986) Acid secretion in some species of Doridacea (Mollusca Nudibranchia). Proc Malacol Soe 38:121-133 Emery KO (1962) Marine geology of Guam. US Geol Surv Prof Paps 403-B 1-76 Evans J.W (1970) Palaeontological implications of a biological study of rock boring clams (Family Pholadidae). In: Crimes TP, Harper JC (eds) Trace fossils. Seel, Liverpool, pp 127-141 Fauchald K (1977) The Polychaete worms. Definitions and keys to the orders, families and genera. Nat Hist Mus Los Angeles Cty Sci Ser 28:188 Finks RM (1970) The evolution and ecologic history of sponges during Palaeozoic times. In: Frey WG (ed) Symposia of the Zoological Society of London, no 25. The biology of the Porifera, pp 3-22 Frith CA, Leis JM, Goldman B (in press) Currents in the Lizard Island Region of the Great Barrier Lagoon and their relevance to potential movements of larvae. Coral Reefs Frydl P (1977) The geological effect of grazing by parrot-fish on a Barbados reef. M Sc thesis, McGill University Frydl P, Stearn GW (1978) Rate of bioerosion by parrotfish in Barbados Reef environments. J Sediment Petrol 48:1149-1157 Ffitterer DK (1974) Significance of the boring sponge Cliona for the origin of fine grained material of carbonate sediments. J Sediment Petrol 44:79-84 Gardiner JS (1902) The action of boring and sand feeding organisms. In: Gardiner JS (ed) The fauna and geography of the Maldive and Laccadive Archipelagoes, vol. 1. Cambridge University Press, Cambridge pp 33-341 Gardiner JS (1903) The origin of coral reefs as shown by the Maldives. Am J Sci 16:203-213 Glynn PW, Wellington GM, Birkeland C (1979) Coral growth in the Galapagos: limitation by sea urchins. Science 203:47-49 Ginsburg RN (1983) Geological and biological roles of cavities in coral reefs. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 148-153 Gohar HAF, Latif AFA (1963) Digestive proteolytic enzymes of some scarid and labrid fishes (from the Red Sea). Publ Mar Biol Stn A1 Ghardaga 12:4M2
251 Golubic S, Perkins RD, Lukas KJ (1975) Boring micro-organisms and microborings in carbonate substrates. In: Frey RW (ed) The study of trace fossils. Springer, Berlin Heidelberg New York, pp 229259 Goreau TF, Hartmann WD (1963) Boring sponges as controlling factors in the formation and maintenance of coral reefs: In: Sognnaes RF (ed) Mechanisms of hard destruction. Publ Am Assoc Adv Sci 75:25-54 Gygi RA (1975) Sparisoma viride (Bonnaterre) the stoplight parrotfish, a major sediment producer on coral reefs of Bermuda? Ecol Geol Helv 68:327-359 Halley RB, Shinn EA, Hudson JH, Lidz B (1977) Recent and relict topography of Boo Bee Patch Reef, Belize. Proc 3rd Int Coral Reef Syrup 2:29-35 Hamner WH, Jones MS (1976) Distribution burrowing and growth rates of the clam Tridacna crocea on interior reef flats. Oecologia 24:207227 Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446-454 Hedley C (1906) The mollusca of Masthead Island, Capricorn Group, Queensland. Part 1. Proc Linn Soc NSW 31:453 Hein FJ, Risk MJ (1975) Bioerosion of coral heads: inner patch reefs, Florida reef tract. Bull Mar Sci 25:133-138 Highsmith RC (1980) Geographic patterns of coral bioerosion: a productivity hypothesis. J Exp Mar Biol Eco146:177-196 Highsmith RC (1981) Lime-boring algae in hermatypic coral skeleton. J Exp Mar Biol Ecol 55:267-281 Highsmith RC, Lueptow RL, Schonberg SC (1983) Growth and bioerosion of three massive corals on the Belize barrier reef. Mar Ecol Prog Sci 13:261-271 Hudson JH (1977) Long-term bioerosion rates on a Florida reef: new method. Proc 3rd Int Coral reef Syrup 2:491-498 Hunter IG (1977) Sediment production ofDiadema antillarum on a Barbados fringing reef. Proc 3rd Int Coral Reef Syrup 2:105 109 Hutchings PA (1974) A preliminary report on the density and distribution of invertebrates living on coral reefs. Proc 2nd Int Coral Reef Symp 1:285-296 Hutchings PA (1978) Non-colonial cryptofauna. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. Monograph on oceanographic methodology, vol 5. UNESCO, Paris, pp 251 262 Hutchings PA (1981) Polychaete recruitment onto dead coral substrates at Lizard Island, Great Barrier Reef, Australia. Bull Mar Sci 31:410M24 Hutchings PA (1983a) Cryptofaunal communities of coral reefs. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 200-208 Hutchings PA (1983b) Bioerosion of coral substrates. In: Baker JT, Carter RM, Sammarco PW, Stark KP (eds) Proceedings of the Inaugural Great Barrier Reef Conference, Townsville 1983. JCU, Townsville, pp 113-119 Hutchings PA (1984) A preliminary report on the spatial and temporal patterns of polychaete recruitment on the Great Barrier Reef. In: Hutchings PA (ed) Proc 1st Int Poly Conf Sydney. Linn Soc NSW, pp 227-237 Hutchings PA (1985) Variability in polychaete recruitment at Lizard Island, Great Barrier Reef: a long term study and an analysis of its potential impact on coral reef ecosystems. Proc 5th Int Coral Reef Symp 5:245-250 Hutchings PA, Bamber L (1985) Variability of bioerosion rates at Lizard Island, Great Barrier Reef: preliminary attempts to explain these rates and their significance. Proc 5th Int Coral Reef Symp 5:333-338 Hutchings PA, Murray A (1982) Patterns of recruitment of polychaetes to coral substrates at Lizard Island, Great Barrier R e e f - an experimental approach. Aust J Mar Freshwat Res 33:1029-37 Hutchings PA, Weate PB (1977) Distribution and abundance ofcryptofauna from Lizard Island, Great Barrier Reef. Mar Res Indonesia 17:99-112 Hutchings PA, Weate PB (1979) Experimental recruitment of endo-cryptolithic communities at Lizard Island, Great Barrier Reef. Preliminary results. N Z Dep Sci Ind Res Inf Ser 137:239556
James NP, Kobluk DR, Pemberton SG (1977) The oldest macroborers: lower Cambrian of Labrador. Science 197:980-983 Jones RS (1968) Ecological relationships in Hawaiian and Johnston Island Acanthuridae (surgeon fishes). Micronesica 4:309-361 Kanwischer JW, Wainwright SA (1967) Oxygen balance in some reef corals. Biol Bull Mar Biol Lab Woods Hole 135:141-148 Kelleher G (1983) Information needs for managing the Great Barrier Reef Marine Park. In: Baker J J, Carter RM, Sammarco PW, Stark KP (eds) Proceedings of the Inaugural Great Barrier Reef Conference, Townsville 1983. JCU, Townsville, pp 43-60 Kiene WE (1985) Biological destruction of experimental corat substrates at Lizard Island, Great Barrier Reef, Australia. Proc 5th Int Coral Reef Symp 5:339-344 Kinsey DW (1983) Standards of performance in coral reef primary production and carbon turnover. In: Barnes DJ (ed) Perspectives in coral reefs. Australian Institute of Marine Science, Townsville, pp 209-220 Kinsey DW, Davies PJ (1979) Carbon turnover, caicification and growth in coral reefs. In: Trudingar PA, Swaine DJ (eds) Biogeochemical cycling of mineral forming elements. Elsevier, Amsterdam, pp 131-162 Kinsey DW (1983) Short-term indicators of gross material flux in coral reefs - how far have we come and how much further can we go? In: Baker JT, Carter RM, Sammarco PW, Stark KP (eds) Proceedings Inaugural Conference, Townsville 1983. JCU, Townsville, pp 333-340 Kleeman KH (1980) Boring bivalves and their host corals from the Great Barrier Reef. J Moll Stud 46:13-54 Kobluk DR, Risk MJ (1974) Devonian boring algae or fungi associated with micrite tubules. Can J Earth Sci 11:1606-1610 Kobluk DR, Risk MJ (1977 a) Calcification of exposed filaments of endolithic algae, micrite envelope formation and sediment production. J Sediment Petrol 47:517-528 Kobluk DR, Risk MJ (1977 b) Rate and nature of infestation of carbonate substrates by a boring algae Ostreobium sp. J Exp Mar Biol Ecol 27:107-115 Kohlmeyer J (1969) The role of marine fungi in the penetration of calcareous substances. Am Zool 9:741-746 Kohn A J, Lloyd MC (1973) Polychaetes of truncated reef limestone substrates on eastern Indian Ocean coral reefs: diversity, abundance, and taxonomy. Int Rev Gesamten Hydrobiol 58:369-399 Kohn AJ, Nybakken JW (1975) Ecology of Conus on eastern Indian Ocean fringing reefs: diversity of species and resources utilization. Mar Biol 29:211-234 Lessios HA, Robertson DR, Cubit JD (1984) Spread of Diadema mass mortality through the Caribbean. Science 226:335-337 Loya Y (1982) Life history strategies of boring bivalves in corals. The reef and man. Proc 4th Int Coral Reef Symp 2:756 (abstr) Lowenstam HW (1962) Magnetite in denticle capping in recent Chitons (Polyplacophora). Bull Geol Soc Am 73:435-438 MacGeachy JK (1977) Factors controlling sponge boring in Barbados reef corals. Proc 3rd Int Coral Reef Symp 2:478-483 Marshall JF (1983) Marine lithification in coral reefs. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 231-239 Marshall JF, Davies PJ (1982) Internal structure and Holocene evolution of One Tree Reef, southern Great Barrier Reef. Coral Reefs 1:21-29 McCloskey LR (1970) The dynamics of the community associated with a marine scleractinian coral. Int Rev Gesamten Hydrobio155:13-81 McLean RF (1967) Measurement of beachrock erosion by some tropical marine gastropods. Bull Mar Sci 17:551-561 McLean RF (1974) Geologic significance of bioerosion of beach rock. Proc 2nd Int Coral Reef Symp 2:401-409 McMichael DF (1974) Growth rate, population size and mantle colouration in the small giant clam Tridacna maxima (Robing) at One Tree Island, Capricorn Group, Queensland. Proc 2nd Int Coral Reef Symp 1:241-245 Neumann AC (1966) Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge Cliona lampa. Limno10ceanogr 11:92-108
252 Ogden JC (1977) Carbonate sediment production by parrot fish and sea urchins on Caribbean reefs. In: Frost SH, Weiss MP, Saunders JB (eds) Reefs and retated carbonates - ecology and sedimentology. Am Assoc Petrol Geol Stud Geol 4:281-288 Ogden JC, Lobel PS (1978) The role of herbivorous fishes and urchins in coral reef communities. Environ Biol Fish 3:49-63 Otter GW (1937) Rock-destroying organisms in relation to coral reefs. Sci Rep Gt Barrier Reef Exped 1:323-352 Peyrot-Clausade M (1974) Ecological study of coral reef cryptobiotic communities: an analysis of the polychaete cryptofauna. Proc 2nd Int Coral Reef Symp 1:269-283 Pomponi SA (1977) Etching cells of boring sponges: an ultrastructural analysis. Proc 3rd Int Coral Reef Symp 2:485-490 Pomponi SA (1979) Ultrastructure and cytochemistry of the etching area of boring sponges. In: Levi C, Boury-Esnault N (eds) Biologie et Spongiaires. Colloques Internationaux du Centre Nationale de la Recherche Scientifique 291:317-323 Purchon RD (1968) The biology of the mollusca. Int Ser Monogr Pure Appl Biol Zool 40:1-560 Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665-847 Randall JE (1974) The effect of fishes on coral reefs. Proc 2rid Int Coral Reefs Symp 1:159-166 Rice ME (1969) Possible boring structures of sipunculids. Am Zool 9:803-812 Rice ME, MacIntyre IG (1982) Distribution of Sipuncula in the coral reef community, Carrie Bow Cay, Belize. In: Rfitzler K, MacIntyre IG (eds) The Atlantic Barrier Reef ecosystem at Carrie Bow Cay, Belize, I. Structure and communities. Smithsonian Institution Press, Washington, pp 311-320 Risk M J, MacGeachy JK (1978) Aspects of bioerosion of modern Caribbean reefs. Revta Biol Trop 26 (Suppl 1):85-105 Risk M J, Sammarco PW (1982) Bioerosion of corals and the influence of damselfish territory. Oecologia 52:376-380 Rooney WS, Perkins RD (1972) Distribution and geologic significance of micro-boring organisms within sediments of the Arlington Reef complex, Australia. Bull Geol Soc Am 83: ! 391-1396 Russ G (1984a) Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef. 1. Levels of variability across the entire continental shelf. Mar Ecol Prog Ser 20:23-34 Russ G (1984b) Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef. II. Patterns of zonation of mid-shelf and outershelf reefs. Mar Ecol Prog Ser 20:35-44 Riitzler K (1974) The burrowing sponges of Bermuda. Smithson Cont Zool 165:1-32 Riitzler K (1975) The role of burrowing sponges in bioerosion. Oecologia 19:203-216 Rfitzler K, Rieger G (1973) Sponge burrowing: fine structure of Cliona lampa penetrating calcareous substrate. Mar Biol 21:144-162 Sale PF (1980) The ecology of fishes on coral reefs. Oceanogr Mar Biol Annu Rev 18:367-423 Sale PF (1983) Temporal variability in the structure of reef fish communities. In Baker JT, Carter RM, Sammarco PW, Stark KP (eds) Proceeding of the Inaugural Great Barrier Reef Conference Townsville 1983. JCU, Townsville, pp 239-244 Sammarco PW (1980) Diadema and its relationships to coral spat mortality. Grazing competition and biological disturbance. J Exp Mar Biol Eeol 45:245-272 Sammarco PW (1982) Echinoid grazing as a structuring force in coral communities: whole reef manipulations. J Exp Mar Biol Ecol 61:3155 Sammarco PW (1983) Coral recruitment across the central Great Barrier Reef: a preliminary report. In: Baker JT, Carter RM, Sammarco PW, Stark KP (eds) Proceedings of the Inaugural Great Barrier Reef Conference, Townsville 1983. JCU, Townsville, pp 245-250 Schultz LP (1958) Review of the parrotfishes, family Scaridae. Bull US Nat Mus 214:1-143
Scoffin TP (1977) Sea-level features on reefs in the northern province of the Great Barrier Reef. Proc 3rd Int Coral Reef Symp 2:319-324 Scoffin JP, Stearn CW, Boucher D, Frydl P, Hawkins CM, Hunter IG, MacGeachy JK (1980) Calcium carbonate budget of a fringing reef on the west coast of Barbados. Bull Mar Sci 30:475-508 Smith RL, Paulson AC (1974) Food transit times and gut pH in two Pacific parrotfish. Copeia 3:769-799 Smith RL, Paulson AC (1975) Carbonic anhydrase in some coral reef fishes: adaptation to carbonate ingestion? Comp Biochem Physiol 50A:131-134 Smith SV (1973) Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol Oceanogr 18:106-20 Soliman GN (1969) Ecological aspects of some coral-boring gastropods and bivalves of the northwestern Red Sea. Am Zool 9:887-894 Stearn CW, Scoffin TP (1977) Carbonate budget of a fringing reef, Barbados. Proe 3rd Int Coral Reef Symp 2:471-476 Stephenson W, Searle RB (1960) Experimental studies on the ecology of intertidal environments at Heron Island. Aust J Mar Freshwater Res 11:241-267 Taylor JD (1971) Intertidal zonation at Aldabra Atoll. Philos Trans R Soc London B Ser 260:173-213 Thompson TE (1960) Defensive acid-secretion in marine gastropods. J Mar Biol Assoc UK 39:115-134 Thompson TE (1961) Acid secretion in British Cowries. Proc Malacol Soc Lond 34:210-211 Thorne MJ (1967) Homing in the chiton Acanthozostera gemmata (Blainville). Proc R Soc Queens179:7%108 Torgersen T, Chivas AR, Chapman A (1983) Chemical and isotopic characterisation and sedimentation rates in Princess Charlotte Bay Queensland. BMR J Aust GeoI Geophys 8:191-200 Trudgill ST (1976) The marine erosion of limestone on Aldabra Atoll, Indian Ocean. Z Geomorphol (Suppl) 26:164-200 Trudgill ST (1983a) Preliminary estimates of intertidal limestone erosion, One Tree Island, Southern Great Barrier Reef, Australia. Earth Surface Proc Landforms 8:189-193 Trudgitl ST (1983 b) Measurement of rates of erosion of reefs and reef limestones. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 256-262 Vivien ML, Peyrot-Clausade M (1974) Comparative study of the feeding behaviour of three coral reef fishes (Holocentridae), with special reference to the Polychaeta of the reef eryptofauna as prey. Proc 2nd Int Coral Reef Symp 2:179-92 Wallace CC (1983) Visible and invisible coral recruitment. In Baker JT, Carter RM, Sammarco PW, Stark KP (ed) Proceedings of the Inaugural Great Barrier Reef Conference, Townsville 1983. JCU, Townsville, pp 259-261 Warme JE (1975) Borings as trace fossils, and the processes of marine bioerosion. In: Frey RW (ed) The study of trace fossils. Springer, Berlin Heidelberg New York, pp 181-229 Warme JE, Marshall NF (1969) Marine borers in calcareous terrigenous rocks of the Pacific Coast. Am Zool 9:765-774 Wilkinson CR (1983) Role of sponges in coral reef structural processes. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 263-274 Wulff JL, Buss LW (1979) Do sponges help hold coral reefs together? Nature 281: 474-475 Yonge CM (1963) The biology of coral reefs. In: Russell FS (ed) Advances in marine biology, vol 1. Academic, New York, pp 209260 Ziegler B, Rietschel S (1970) Phylogenetic relationships of fossil calcisponges. In: Frey WG (ed) Symp Zool Soc London 25:23-40 Zottoli RA, Carriker MR (1974) Burrow morphology, tube formation, and microarchitecture of shell dissolution by the spionid polychaete Polydora websteri. Mar Bio127:307-316
Note added in proof Recently, massive mortality of Diadema antillarum has been reported from the Caribbean (Bak et al. 1984; Lessios et al. 1984) and Bak has subsequently studied the impact of this mortality on recruitment succers (Bak 1985).
