DISTRIBUTION, HABITAT AND MORPHOLOGY OF THE CARIBBEAN CORAL- AND ROCK-BORING BIVALVE,LITHOPHAGA BISULCATA (d'ORBIGNY) (MYTILIDAE: LITHOPHAGINAE)

Lithophaga bisulcata is the most common Caribbean and Atlanticlithophagine and is the only species of the genus known to occurfrequently in both living and dead coral. The abundance in livingcorals is non-random and variable. Most common hosts are Siderastereasiderea and Stephanocoenia michelini. The bivalves are moreabundant in their preferred hosts than in dead coral. Individualsfrom the two habitats are indistinguishable in shell shape,musculature and size of boring and posterior pallia! glands,indicating a single population. Boreholes differ in the twohabitats with respect to size and lining. Linings are formedat the "inactive" end of the burrow; therefore living coralinhabitants line the anterior end of the burrow and dead coralborers line the posterior end. Recruitment rates are unknownin dead coral but were very low in living coral (Received 9 June 1987;     

A NEW SPECIES OF LITHOPHAGA (BIVALVIA: LITHOPHAGINAE) BORING CORALS IN THE CARIBBEAN

A new species of Lithophaga is described as a small lithophaginemussel exclusively boring Madracis mir-abilis, M. decactis andM. formosa in Jamaica. The shell, musculature and pallial glandsshow modifications for live coral boring similar to those ofIndo-Pacific species of the genus. However, both the boringand posterior pallial glands are more primitive than other speciesexamined to date, interpreted as indicative of a more recentadaptation to life in a living coral habitat by this species. ^*Contribution No.359 of the Discovery Bay Marine Laboratory,University of the West Indies (Received 23 April 1985;     

Morphological and functional specializations of the shell, musculature and pallial glands in the Lithophaginae (Mollusca: Bivalvia)

The structure of the pallial glands in limestone and coral boring species of Lithophaga (Bivalvia: Lithophaginae) is examined and related to evolutionary trends in habitat specialization. Boring glands of all species occur in the middle mantle fold but display a progressive degree of complexity from simple epithelial to ducted sub-epithelial structures coinciding with increasing specialization of habitat from natural limestone to species specific live coral dwellers. The size of this gland is relatively reduced anteriorly and along the entire length of the mantle in live coral borers.     

Boring by Macro-organisms in the Coral Montastrea annularis on Barbados Reefs

The fauna boring into Montastrea annularis includes sponges, bivalves, sipunculid and polychaete worms and barnacles. Sponges are most important in hard tissue destruction and account for more than 90% of the total boring in most heads. Bivalves and barnacles are locally important. Sipunculids and sabellids account for less than 4% of the total boring. The volume removed from coral samples by boring ranged from 3–60% and samples from a deeper bank reef were more highly bored than fringing reef samples. An average of 20% of the volume of bank reef corals, and 5% of the volume of fringing reef corals, was removed by boring. The distribution of individual borers is not a function of depth. The density and variety of borers and the extent of boring in coral heads is greater in older heads. The ratio of living coral surface to dead encrusted areas on colonies also influences borer density and the extent of boring.     

Bioerosion experiments at Lizard Island,Great Barrier Reef

The rates at which dead coral substrates are modified by bioerosional processes were determined by exposing recently killed corals for up to four years in a variety of reef environments at Lizard Island (northern Great Barrier Reef). Grazers were the major croding agents of these coral substrates and exhibited differences between sites that varied between sampling periods. Subtidal reef slopes and lagoon environments of water depths < 20 m were subjected to higher average rates of grazing erosion (0.30–1.96 kg/m²/y) than shallow depths less than 1 m (0.07–0.26 kg/m²/y). A deep site at 20 m experienced low average rates of grazing (0.08–0.29 kg/m²/y). Boring rates by worms (polychaetes and sipunculans), sponges and molluscs were relatively low and varied between sites, but increased with length of sampling period as larger borers succeeded the initial colonizing small polychaete worms. We hypothesize from these experiments that the extent of boring in reef substrates will be influenced by the interaction between the succession of the boring community and the rate at which the substrate is destroyed by grazing. We suggest that the level of grazing modifies the successional pattern of borers by removing the surface substrate and continually exposing bare substrate that can be colonized by early boring colonists. Thus, constant high levels of grazing may maintain the boring community at an early successional stage and prevent the development of a mature boring community. In order to establish large borer populations, reef substrates must be protected from extensive grazing bioerosion. This interaction of grazing and boring has important implications for the way dead coral is preserved in different reef environments.     

Borers in the Shell of the Sea Scallop, Placopecten magellnnicus

Shells of the sea scallop, Placopecten magellanictis Gmelinfrom Newfoundland waters were examined for borers by directstereomicroscopic and X-ray radio-graphic means. Young shells are first attacked by the boring sponge, Clionavastifica, and the spionid polychaetes, Polydora websteri andPolydora concharum. The former settles almost exclusively onthe lower valve, but as it grows it often spreads to the uppervalve via the hinge region. The spionids settle on the uppervalve or occasionally on the periphery of the lower valve. Older shells are bored by the cirratulid polychaete, Dodecaceriaconcharum, which usually settles in empty Polydora burrows andenlarges them as they grow. The bivalve, Hiatella arctica, settlesin Cliona holes. The burrows formed by the borers can be recognized on the radiographs.However, the identity of the present inhabitant cannot be predictedwith accuracy because the original borer is often replaced bynestlers. The rale of growth was documented by making sequential radiographsat monthly intervals from May to October 1968. Rate of growthin all forms appears to be temperature-dependent. The watertemperature increased from 1°C in May up to 18°C inAugust. Polydora concharum and P. websteri grew more rapidlyfrom July to October than in Mayand June, while Cliona and Dodecaceriaonly grew during the months of July to October.     

EVIDENCE FOR CHEMICAL BORING IN PETRICOLA LAPICIDA (GMELIN, 1791) (BIVALVIA: PETRICOLIDAE)

Specimens of the dead coral-boring bivalve Petri-cola lapicidahave been obtained from Thailand and Jamaica. Although formerlyconcluded to be a mechanical borer, examination of the burrowand the shell strongly suggests chemical boring. Two glandslocated in the inner mantle folds around the antero-ventr'alpedal gape are thought to be involved in this, although onemay secrete the calcareous material cemented to the posteriorshell margin Less specialised petricolids are mechanical borers of stiffmuds, shales and calcareous rocks. A few are nestlers, e.g.,Claudiconcha. As has been recently suggested for other familiesof borers, the Petricolidae constitute another example of theevolution of a specialised chemical borer from a less specialisedmechanically-boring ancestor (Received 20 July 1987;     

Bioerosion of gastropod shells: with emphasis on effects of coralline algal cover and shell microstructure

Organisms boring into fifty nine species of gastropod shells on reefs around Guam were the bryozoan Penetrantia clionoides; the acrothoracian barnacles Cryptophialus coronorphorus, Cryptophialus zulloi and Lithoglyptis mitis; the foraminifer Cymbaloporella tabellaeformis, the polydorid Polydora sp. and seven species of clionid sponge. Evidence that crustose coralline algae interfere with settlement of larvae of acrothoracian barnacles, clionid sponges, and boring polychaetes came from two sources: (1) low intensity of boring in limpet shells, a potentially penetrable substrate that remains largely free of borings by virtue of becoming fully covered with coralline algae at a young age and (2) the extremely low levels of boring in the algal ridge, a massive area of carbonate almost entirely covered by a layer of living crustose corallines. There was a strong negative correlation between microstructural hardness and infestation by acrothoracian barnacles and no correlation in the case of the other borers. It is suggested that this points to a mechanical rather than a chemical method of boring by the barnacles. The periostracum, a layer of organic material reputedly a natural inhibitor of boring organisms, was bored by acrothoracican barnacles and by the bryozoan. The intensity of acrothoracican borings is shown to have no correlation with the length of the gastropod shell.     

Boring Mechanism of Polydora websteri Inhabiting Crassostrea virginica

The boring mechanisms of species of polydorid polychaetes arelittle understood due to lack of experimental evidence and directobservations. In the present studies the boring mechanism ofadults and metamorphosing larvae of Polydora websteri was investigatedby (1) inducing adults and larvae to settle against test substrates,(2) observing behavior in natural burrows and in "artificialblisters" composed of transparent "Pliobond" films surroundingIceland spar substrates, (3) removing the giant setae of wormspriorto tests of boring, (4) applying the giant setae to substrates,and by (5) testing for production of acid. All the layers of oyster shell, including conchiolin, were bored.Calcareous substrates andIceland spar were penetrated rapidlyby adults without the assistance of the giant setae. Nor werethese organs essential to the boring of a larva. A characteristictype of behavior involving close contact with the substrateduring backwards and forwards movements and periods of immobilityalways preceded boring. The worms produced acid, probably somecommon product of metabolism, which can account for these results.     

A Comparative Study of Bivalves Which Bore Mainly by Mechanical Means

This account of the boring mechanisms of those bivalve groupswhich bore mainly by mechanical means attempts to show partlyby reference to published accounts of boring and partly fromour own recent observations of certain characteristics of theboring process in the Pholadidae and Petricolidae, that in contrastto the movements of burrowing forms from which originally allthe boring movements derive, the process of boring makes fewdemands on the hydrodynamic system of the bivalve. The characteristicsof the boring process are closely related to the movements inmodern forms having epifaunal or infaunal habits, supportingthe suggestions of Yonge (1963) concerning the origin of thishabit in the Bivalvia. In all groups in which boringis mechanical,the shell forms the boring tool. However, in those groups inwhich boring has its origin in the epifaunal habit, the majorforce applied to the shell in abrading the burrow isprovidedby contractions of the pedal or byssal retractor muscles. Inthe Adesmacea alone, where boring has been derived from a deepburrowing habit, the adductor muscles provide the major forcein abrasion, and the basic digging cycle has become specializedby the addition of the rocking action of the valves which succeedsretraction. In the former group the ligament is retained andprovides the strong outward force with which the shell is heldagainst the wall of the burrow. In the latter group, the ligamentis reduced, allowing the valves to rock, but here the reciprocalaction of the adductors allows the valves to diverge anteriorlyas the large posterior retractor muscle contracts. In the morespecialized species, water pressure plays a minor role, themaximum pressures recorded being associated with actions subordinateto those involved primarily in abrasion, such as rotation inthe burrow or expulsion of debris from the burrow aspseudofeces.The least specialized borers, such as Petricola, resemble burrowingforms in the importance of the hydrodynamic role of the bodyfluids. In all groups there is a tendency for hypertrophy totake place in the muscles which produce the main boring effect,and for their action to be applied with maximum mechanical advantageagainst a fulcrum provided in most cases by the foot.     

Associations of corals and boring bivalves since the late cretaceous

Summary The fossil record of coral and boring mytilid bivalves IS investigated. Middle Miocene associations from Austria, Hungary, and Turkey are described. As host corals,Montastrea, Porites, Siderastrea, Solenastrea, andTarbellastraea can be noted. Eocene (Waschberg Zone) and Upper Cretaceous (Gosau Formation) examples are presented from Austria only. As host corals,Favia andMontastrea, respectivelyAstrocoenia and an unidentified branching coral are recorded. The associated bivalve species are all mytilidLithophaga, includingL. laevigata (Quoy & Gaimard) inTarbellastraea, a new Middle Miocene species inMontastrea, andL. alpina (Zittel) inAstrocoenia, the latter two from Styria, Austria. Thecharacteristic features of the coral-bivalve relationships include (in massive corals): Boreholes more or less in the direction of coral growth, radially arranged, elongate boreholes, produced by keeping pace with coral growth. Bivalves were not only present near the surface, but deep inside the skeleton, representing successive generations in the same host colony. After the death of borers, their tunnels were closed by coral overgrowth. Cup-shaped false floors in the boreholes are correlated to reduced coral growth, indicating individual longevity of bivalves. The spacing of the floors mirrors the growth rate of the host coral (like its density bands), their number representing the minimal age of the respective bivalve. In branching corals, boreholes of the associated smallsizedLithophaga tended to turn into the axes of branchlets, when space was limited. Elongated boreholes and false floors were usually not developed, as bivalve growth obviously exceeded lateral growth of branchlets and specimens were rather short-lived. References to probable associations of coral and mytilid boring bivalves are given. It is quite likely that they have occurred since Jurassic times and probably since the Upper Triassic. So far, they have been ascertained since the Upper Cretaceous in massive and branching corals.     

INITIAL SETTLEMENT BEHAVIOUR AND SURVIVORSHIP OF LITHOPHAGA BISULCATA (d'ORBIGNY) (MYTILIDAE: LITHOPHAGINAE)

Although infaunal associates of living reef building coralsindude numerous phyla, initial settlement on the coral hosthas never been described. Experiments described here includedraising the larvae of a common Caribbean coral-boring mussel,Lithophaga bisulcata to observe their behaviour in the presenceof a variety of settlement substrates. On Stephanocoenia michelini,the most common host, larvae moved about the coral surface withimpunity, exploring the surface with the foot. On this coralspecies, competent pedi-veligers were ingested by the coralbut not necessarily digested. Penetration of the coral is initiatedby entering the coelenteron, where metamorphosis will presumablytake place. On species which L. bisulcata rarely inhabits, thelarvae appeared to be stung by nematocysts and withdrew thefoot rapidly from contact with the tissue Habitation of a living coral substrate appeared to be beneficialto the bivalve. Although L. bisulcata inhabits both riving anddead coral, there is evidence that survival, longevity and reproductiveoutput are enhanced when the mussel is surrounded by livingcoral tissue (Received 9 June 1987;     

Developments in the understanding of the biology of marine wood boring crustaceans and in methods of controlling them

The most economically important wood boring Crustacea belong to the isopod families Sphaeromatidae and Limnoriidae, both of which have been recently revised and a number of new species have been recognised. Other wood boring crustaceans have now been recognised from tropical mangrove sites. Limnoriids are found from temperate to tropical waters, but appear to be restricted to waters with salinities close to that of seawater. Wood-boring species of Sphaeroma on the other hand can tolerate extremely low salinities, but are restricted to sub-tropical and tropical waters. Approaches to borer control that have proved effective against teredinids (use of naturally durable timber, copper-chrome-arsenic or creosote treatment, surface coatings) have been found under certain circumstances to be ineffective against Limnoria and Sphaeroma. A number of additives to conventional preservatives have been tested, with some insecticides showing evidence of enhancing Limnoria control. The question of crustacean borer nutrition may hold the key to problems of their control. Sphaeromatid borers are capable of filter-feeding and thus may never ingest the treatments applied to wood. Limnoriids do ingest wood, but the role of wood degrading tunneling bacteria, and soft-rotting ascomycete and deuteromycete fungi occurring in the wood they digest remains to be fully elucidated. The source or sources of wood-degrading enzymes that permit digestion of wood particles requires further investigation. The microecology of borer burrows has an important bearing on the availability of nitrogen for borers. Further insights into the problems posed by these borers may be obtained with a better understanding of their ecology. A better testing protocol for preservatives has been developed as a result of knowledge of the natural vertical distribution of Sphaeroma. Behavioural studies indicate that settlement on wood by Limnoria is enhanced by factors derived from conspecifics and from wood-inhabiting microorganisms.     

Functional Morphology of Perihelia conradi Relative to Shell-Penetration

The pholad, Penitella conradi, is found along the Californiacoast in the calcareous shell of the abalone, Haliotis rufescens.These pholads penetrate the abalone shell, and when they breakthrough the inside of the shell they cease boring, secrete acallum, and then become sexually mature. The normal adult isa stenomorphic form,defined by Bartsch as an animal whose sexualmaturity is induced by over-crowding or insufficient substratumin which to bore. In the case of P. conradi, sexual maturityis always induced by the spatial limits of the substratum, thatis, the relatively thin abalone shell. The role of mechanical abrasion by the valves of P. conradiis minor. Experiments indicate that the teeth of P. conradiare worn at a greater rate than the polished shell of the abalone. The boring process in P. conradi proceeds mainly by chemicaldissolution of the calcareous substrate. The pathway of thesolvents is unknown. It may be through the organic matrix, orthe solvent may react directly with the crystals. Mechanicalabrasion helps to remove loosened crystals and/or organic matrixwhich are then carried to the exterior by the ciliary currentsflowing in through the pedal gape and out through the exhalentsiphon.     

Possible Boring Structures of Sipunculids

At the present time there is no experimental evidence whichlinks the supposed boring activities of sipunculids to a specificorgan or structure. Structures which have been speculativelyassociated in the literature with boring are: hooks and spinesof the introvert, cuticular papillae with associated epidermalglands, anterior and posterior horny shields, and anterior calcareousshields. In this review these structures are described as theyoccur in five representative species of sipunculids collectedby the author from calcareous rock in the Indian Ocean or theCaribbean Sea. The five species are: Pliascolosoma antillarumGrube and Oersted, Phascolosoma dentigerum (Selenka and de Man), Paraspidosiphon steenstrupi (Diesing), Lithacrosiphon gurjanovaeMurina, and Cloeosiphon aspergillum (Quatrefages). Localitiesof collections are cited, habitats and burrows are described,and the behavior of the animals as observed in the field andlaboratory is noted. In view of the morphology of the possibleboring structures and in light of observations on habitats andbehavior, the possible roles of the structures in boring activitiesare discussed. Highly organized horny shields are present at the anterior andposterior extremities of thetrunk or Paraspidosiphon steenstrupi,whereas anterior calcareous shields are characteristic of Cloeosiphonaspergillum and Lithacrosiphon gurjanovae. Papillae and epidermalglands are present in all five of the species but these aremost highly developed in Phascolosoma dentigerum and P. antillarum.Of the species considered, only P. antillarum lacks hooks onthe introvert. Because of the position of the animal within the rock with anteriorend directed toward themouth of the burrow, it is assumed thatthe anterior shields and the hooks of the introvert play nosignificant role in the formation of the burrow. However, therigid papillae of the trunk and the thickened posterior shield,if rubbed against the wall of the burrow, presumably could beutilized in the mechanical attrition of the more friable rock,whereas the secretory products of the numerous epidermal glandsmight be implicated in the chemical dissolution of the hardersubstrates.     

Geographic patterns of coral bioerosion: A productivity hypothesis

The numbers of boring bivalves in corals in large museum collections were used to indicate relative bioerosional damage to the corals. The proportion of corals from different locations that contain boring bivalves is highly correlated with global patterns of plankton primary productivity. The densities of five other, non-boring, groups of plantivores associated with the same corals are similarly correlated with productivity.The proportion of corals containing boring bivalves and the number of boring bivalves per coral head can be ranked by region as follows: eastern Pacific > western Atlantic > Indian Ocean > western Pacific. This ranking also corresponds to primary productivity differences.Measurements of the basal, margin of live tissue, and maximum circumstances of the coral heads indicate that western Atlantic massive corals have more of their skeletal surface exposed to borers, i.e. not covered by live tissue, than do Indo-Pacific corals. Consequently, the former also have weaker basal attachments which suggests that they are more likely to be dislodged during storms. The reason why massive corals in the western Atlantic tend to have less of their skeleton covered by live tissue than corals in the rest of the world is unknown.     

Temporal variations of macroborers in massive Porites lobata on Moorea,French Polynesia

Massive colonies of Porites lobata on the barrier reef of Tiahura, Moorea, can be divided into four categories: living colonies, colonies consisting of 50% live coral and 50% dead skeleton, 100% dead coral and colonies which have been reduced to a basal plate. Replicate samples of each of these colony types were collected in the same vicinity of the barrier reef during October 1987. The macroborers were extracted, identified, counted and their volumes determined by displacement. Kruskal-Wallis tests showed that three different boring communities occur within these four categories of Porites colonies. Live colonies are characterised by only 3 species, the bivalve, Lithophaga laevigata; the vermetid Dendropoma maximun; and the non boring serpulid polychaete Spirobranchus. The completely dead colonies contain up to 17 boring species, with five to six individuals per 100 cm. Sipunculans are the dominant bioeroders with the most abundant species being Aspidosiphon elegans, sp A and sp B. Colonies of Porites which have been reduced to basal plates contain up to 18 boring species of which the bivalve Lithophaga hanleyana and the sipunculan Aspidosiphon sp. B are the most abundant.The cumulative volume of CaCO₃ lost by boring activity increases from 0.1 cm³ per 100 cm³ in a completely dead Porites colony to 1.4 cm³ per 100 cm³ in the residual basal plates of Porites. These can be extrapolated to minimum losses of 14.2 kg m^-3. We suggest that rates of boring increase with the time which has elapsed since the death of the colony and the dominant agents of boring also change with increasing age of the coral structure. There are significant additional losses of 5.25 kg m^-3 CaCO₃ caused by grazing echinoids and scarids.     

Response of Pleistocene Coral Reefs to Environmental Change Over Long Temporal Scales

SYNOPSIS. TWO studies from the Pleistocene coral reef fossilrecord demonstrate the sensitivity of reef communities to bothlocal environmental parameters and habitat reduction. In thefirst study, Pleistocene reef coral assemblages from Papua NewGuinea show pronounced constancy in taxonomic composition andspecies diversity between 125 and 30 ka (thousand years). Spatialdifferences in reef coral community composition during successivehigh stands of sea level were greater among sites of the sameage than among reefs of different ages, even though global changesin sea level, atmospheric CO₂ concentration, tropical benthichabitat area, and temperature varied at each high sea levelstand. Thus, local environmental variation associated with runofffrom the land had greater influence on reef coral communitycomposition than variation in global climate and sea level.Proportional sampling from a regional species pool does notexplain the temporal persistence and local factors likely playeda major role. Examination of coral reef response to global changeshould not only involve regional diversity patterns but alsolocal ecological factors, and the interactive effects of localand global environmental change. In the second study, Pleistocene extinction of two widespread,strictly insular species of Caribbean reef corals, Pocilloporacf. palmata (Geister, 1975) and an organ-pipe growth form ofthe Montastraea "annularis" species complex, was natural anddid not involve gradual decrease in range and abundance, butwas sudden (thousands of years) throughout the entire range.One explanation is that sea level drop at the Last Glacial Maximum(LGM—18 ka) resulted in a threshold of habitat reduction,and caused disruption of coral metapopulation structure. Thresholdeffects predicted by metapopulation dynamics may also explainthe apparent paradox of the large amount of degraded modernreef habitat without any known modern-day reef coral extinctions.The rapid extinction of widespread Pleistocene species emphasizesthe vulnerability of reef corals in the face of present rapidenvironmental and climatic change.     

Skeletal response of <Emphasis Type="Italic">Lophelia pertusa</Emphasis> (Scleractinia) to bioeroding sponge infestation visualised with micro-computed tomography

The skeleton morphology of the azooxanthellate cold-water coral Lophelia pertusa can be strongly influenced by invasive boring sponges that infest corallites in the still living part of the colony. Atypically swollen corallites of live Lophelia pertusa from the Galway Mound (Belgica Carbonate Mound Province, Porcupine Seabight, NE Atlantic), heavily excavated by boring organisms, have been examined with a wide range of non-destructive and destructive methods: micro-computed tomography, macro- and microscopic observations of the outer coral skeleton, longitudinal and transversal thin sections and SEM analyses of coral skeleton casts. As a result, three excavating sponge species have been distinguished within the coral skeleton: Alectona millari, Spiroxya heteroclita and Aka infesta. Furthermore, four main coral/sponge growth stages have been recognised: (1) cylindrical juvenile corallite/no sponge cavities; (2) flared juvenile corallite/linear sponge cavities (if present); (3) slightly swollen adult corallites/chambered oval sponge cavities; (4) very swollen adult corallites/widespread cavities. The inferred correlation between corallite morphology and boring sponge infestation has been detected in micro-computed tomography (micro-CT) images and confirmed in sponge trace casts and peculiar features of coral skeleton microstructure. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorised users.