Morphology and Life Habits of the Recent Cementing Bivalve Spondylus Americanus Hermann from the Bermuda Platform1

MORPHOLOGY AND LIFE HABITS OF THE RECENT CEMENTING BIVALVE SPONDYLUS AMERICANUS HERMANN FROM THE BERMUDA PLATFORM1

A. LOGAN Department of Geology, University of New Brunswick, Saint John, N. B., Canada

ABSTRACT The morphology, ontogeny, distribution and life habits of the thorny oyster Spondylus american us Hermann from the Bermuda Platform have been investigated, with a view to aiding paleoecological reconstructions in fossil relatives. The species is ubiquitous over a wide variety of environments throughout the Platform, but its distribution is primarily controlled by the availability of a suitably firm coral-encrusted substrate. Five main modes of life of S. americanus occur: 1) cemented to the exposed, steep face of coral reef masses; 2) attached to the roof and walls of crevices and cavities in the reef, where it forms part of the cryptofauna; 3) cemented to the lee side of foliaceous corals, particularly Agaricia fragilis, where it is typically associated with an algal-foraminiferal- brachiopod-bryozoan cryptic assemblage; 4) within the abandoned concave valves of earlier-generation S. americanus in shell beds; 5) lying free in sediment pockets and sand channels, having been dislodged from its cemented habit by storms or predators. The paradigmatic approach to functional morphology has been utilized to ascribe likely functions to the various spine types in S. americanus. Finally, the main taphonomic processes responsible for the reduction of the spondylid shell to skeletal detritus have been discussed and evaluated.

INTRODUCTION Although the basic anatomy of most modern bivalves is reasonably well known, ecological observations are generally insufficient for use in paleoecological reconstructions. This is partly because biologists in the past have tended to regard such data as relatively unimportant in their studies. Yet comprehensive data on the requirements of present-day bivalves pro- vide the paleoecologist with information which is essential for comparative anatomical studies and analyses of functional morphology of the bivalve shell. The importance of such observations in "interpretive paleontology" has been stressed by Carter (1967) and Kauffman (1969) and detailed studies of bivalve life habits are beginning to appear in the literature (e.g. Bretsky, 1967; Stanley, 1970). In a masterly exposition on form, function and evolution in bivalves, Kauffman (op. cit. p. N134) has cited the most neglected aspects of Recent bivalve ecology as: "1) the lack of data con-

1 Contribution No. 581 of the Bermuda Biological Station. Manuscript accepted July 24, 1973. 1974] Logan: Morphology and Life Habits of Spondylus americanus 569 ceming behavior; 2) the paucity of community studies and ecologic inter- relationships within communities; 3) general lack of knowledge concerning ecological control on morphologic variation; 4) almost total absence of data on how living communities of animals are reflected in shell accumula- tions of the substrate (the potential fossil deposits) with which they are associated." Carter (1967, p. 70) also maintains that "the lack of pub- lished information on the anatomy and habits of spectacular tropical mollusca remains as one of the largest gaps in modern understanding of invertebrate biology. Yet the functional interpretation of fossil and Recent Bivalvia is critically dependent upon the amount of information available on the biology of Recent species." It may be thought that the life habits of cemented fossil bivalve species can be ascertained without the necessity for comparison with living forms, as these forms are commonly fossilized in situ (Stanley, 1970). This is partly true, yet knowledge of the basic life habits itself is surely insufficient. What, for instance, was the functional significance of the spines, not only in fossil spondylids, but in other less closely related forms, such as hermatypic pseudomonotids and aviculopectinids, which share this structural similarity with Spondylus? Kauffman (op. cit.) has pointed out the presence of adaptive homeomorphy in bivalves and stressed the importance of interpreting the functional morphology of extinct groups in the light of its adaptive value in living homeomorphic (but not necessarily phylogeneti- cally-related) counterparts. This paper, then, discusses the anatomy, shell microstructure, ontogeny, life habits and taphonomy of the warm-water cemented bivalve Spondylus americanus2, known as the Atlantic Thorny Oyster, from Bermuda. Some discussion on the functional aspects of certain features of this species is also included, in the hope that the conclusions drawn may aid in interpretation of function of analogous structures in related and unrelated fossil groups.

GENERAL REMARKS ON SPONDYLIDAE In the most recent classification of the Bivalvia (Newell, 1969) the family Spondylidae is included within the superfamily Pectinacea of the order Pterioida. The family extends as far back as the Jurassic and all members are cemented, for at least a part of their existence, to the substrate, while most are spinose. Nicol (1964, 1965) and Stanley (1970) have pointed out that cementation and spine development require extra amounts of calcium carbonate in sea water, a condition encountered in

"Some authorities prefer the specific epithet iclericlIs Reeve for the common Spondyills of Florida and Bermuda. However, pending a complete systematic revision of Atlantic spondylids, including re-examination of the type specimens of all species, the more familiar name american liS is retained throughout this paper. 570 Bulletin of Marine Science [24(3) many shallow tropical marine areas at the present time. This may account for the essentially pantropical distribution of Recent species of Spondylus. The general characters of the spondylid group are fairly well known. Briefly, Spondylus is an epifaunal, filter-feeding, spinose to concentrically- foliaceous cemented member of the benthos, characterised by a pleurothetic attitude and a resultant inequivalve condition, the larger or right valve being the lower or attached valve. A triangular cardinal area is present in both valves, but is larger in the attached valve. The areas enclose a recessed resilifer containing a narrow alivincular resilium, while the den- tition is isodont. The musculature is monomyarian. The foot is reduced following initial cementing activity. Sensory tentacles and eyes, the latter responsible for a marked shadow reflex reaction, are present along the mantle edge of both valves, except in the fused areas near the hinge extremities. The evidence for the inclusion of Spondylus within the Pectinacea has been documented by Jackson (1890), Dakin (1928a, 1928b) and more recently by Newell and Boyd (1970). The ontogenetic, anatomical and paleontological evidence for this relationship is unequivocal and has recently been further supported by shell microstructure studies by Taylor, Kennedy and Hall (1969). Newell and Boyd (1970), using all available evidence, have postulated an approximate morphologic and phyletic series linking Jurassic Spondylus with Late Paleozoic Pseudomonotis by way of Pro- spondylus (Permian), Paleowaagia (Permian) and Newaagia (Triassic).

MORPHOLOGY OF Spondylus american us The basic anatomy of the type species S. gaederopus Linne was described and illustrated by Dakin (1928a). The anatomy of S. americanus is similar to that of the type species and needs only slight elaboration here, following a recent description by Yonge (1973). Mantle Edge Relationships, Shell Structure and Mineralogy.-In S. americanus the mantle edge is subdivided into three folds, much as Dakin (1928a) described it for S. gaederopus. The outer mantle fold is separated by a narrow periostracal groove from the middle sensory fold bearing tentacles and eyes (Fig. 1). A definite periostracum was not seen, however, although presumably an inconspicuous or perhaps periodic periostracum must form to act as a substrate for initial secretion of outer shell layer. The inner mantle fold contains radial muscles which are attached to the interior of the shell along the pallial line. A well-developed, black-brown striped velum is formed from inner mantle fold material and is present as a curtain in each valve around the whole perimeter of the shell, except near the hinge line, where the margins are fused. The shell structure and mineralogy of members of the Spondylidae have been described in detail by Bl1lggild (1930) and Taylor et al. (1969). 1974] Logan: Morphology and Life Habits of Spondylus americanus 571

middle aragonitic crossed - lamellar layer

FIGURE 1. Radial section of Spondyills anrericanus showing shell layers and mantle edge. AS = limits of adductor muscle scar; C = 'catch' muscle scar; Q = 'quick' muscle scar; PL = pallial line; 0 = outer mantle fold; pg = periostracal groove; m = middle mantle fold with sensory organs; i = inner mantle lobe, of striped velum. X 1.5.

B0ggild distinguished an outer foliated calcitic layer, followed by two aragonitic layers, the uppermost crossed-lamellar and the lowermost prismatic, in the species of Spondylus which he studied. Taylor et al. examined four species of Spondylus, including the type species S. gaederopus, but not S. american us. The five layers recognized by these authors in their study are present in S. american us (Fig. 1) and are briefly described below: A) OUTER CALCITIC FOLIATED LAYER: The outer layer of the shell, including the spines and frills of both valves, is made up of lenticular laths of calcite, often inclined at high angles to the inner boundary of the layer, especially towards the ventral margins of the shell. This layer is easily recognized in Spondylus american us, as it contains a color pigment varying from red-orange to yellow. Comfort (1951) has suggested that color pigmentation in bivalves results from the secretion of metabolic waste products; certainly in S. american us the coloration can have no primary camouflagic function, as the shell surface is usually heavily encrusted with epibionts. B) MIDDLE ARAGONITICCROSSED-LAMELLARLAYER: This layer, which forms the hinge and teeth as well as the internal area beyond the pallial line, is made up of concentrically-arranged first-order lamellae which are easily seen, even without sectioning, in well-preserved juvenile specimens of Spondylus american us. The nature of the crossed-lamellar structure has been described in detail by Taylor et al. (1969) and no further mention needs to be made of it here. c) ARAGONITICPRISMATIC PALLIAL MYOSTRACALLAYER: Taylor et al. e 1969) have used the term "myostracum" for prismatic aragonite shell substance laid down beneath areas of muscle attachment and their usage 572 Bulletin of Marine Science [24(3) is followed here. The track of the pallial muscle attachment (pallial line) is very thin in S. americanus except in the area of the present pallial line, in the last-formed part of the shell, where the myostracum has a zig-zag contact with the overlying middle crossed-lamellar layer. In this region the lower boundary of the pallial myostracum is irregularly extended downwards into the underlying inner crossed-lamellar layer by prismatic myostracal "pillars" and is difficult to delimit exactly. Taylor et al. (1969, p. 98, fig. 60) illustrate the pallial myostracum in S. calcifer as a thin layer between two structurally-continuous crossed-lamellar layers, but the pallial myostracum in S. americanus separates middle crossed-lamellar layer from adductor myostracum for most of its length. D) ARAGONITICPRISMATICADDUCTORMYOSTRACALLAYER: This layer outcrops on the interior of the shell within the limits of the adductor muscle scar and consists of small scale-like crystals of aragonite forming a thick band representing the growth track of the adductor muscle attachment. For much of its length it is in contact upwards with prismatic pallial myostracum of similar appearance and the two layers are thus often difficult to distinguish. As in the pallial myostracum the lower boundary of the adductor myostracum may invade the inner crossed-lamellar layer by means of myostracal "pillars" which are probably responsible for the ring- like structures seen on the interior of the shell in well-preserved S. american us. Within the adductor myostracal layers there is a faint trace of the boundary between the "quick" and "catch" segments of the adductor muscle. E) INNER ARAGONITICCROSSED-LAMELLARLAYER: Strong banding, especially below the hinge area, is typical of this layer and may represent thin myostracal bands of former mantle attachment, as suggested by Taylor et al. (1969). The upper part of the inner crossed-lamellar layer is usually penetrated by pillars from the overlying myostracallayers and may become almost completely replaced by them. Very small discontinuous perfora- tions or micro-canals ("tubules" of Taylor et al.) are well shown in this layer and have been described in detail by Omori and Kobayashi (1963) and Taylor et al. (1969). While their exact function is not entirely under- stood, they are thought to contain organic materials during life. Ontogenetic Development.-Because of the short period during which S. americanus could be observed in the laboratory, little information is available on spawning and larval development in this species. The sexes are separate in this species and specimens dissected in July, 1971 showed ripe gonads but spawning was not directly observed. Bullivant (1962) reported direct observation of spawning in Spondylus sp. from an atoll in the Northern Cook Group in August, but attributed it to unusually warm water conditions at that time. 1974] Logan: Morphology and Lite Habits ot Spondylus americanus 573 Nothing is known of the period between fertilization of the egg and settling of the spat, although presumably the stages described by Gutsell (1931) for the scallop Pecten irradians are similar to those undergone by Spondyilis. It is likely, however, that the veliger larva in Spondylus, as in several other bivalve species, is selective in choosing a suitable substrate for settlement (Thorson, 1946, 1966; Wilson, 1952). Following metamorphosis an initial period of byssal attachment is implied by the presence in all spondylids of a marked byssal notch in the early-prodissoconch shell of the attached valve. This nepionic growth form in both valves is represented by a zone of essentially smooth shell about 1.5-2.0 mm in height. During this stage the non-spinose spondylid spat are members of the meiobenthos, albeit for a short time, and are vulnerable to both macro- and micro-predators (Thorson, 1966). Cementation to the substrate soon follows, as shown by the presence of coarse foliaceous growth increments around the uncemented juvenile part of the shell. At this point the abandoned byssal notch is infilled with foliaceous shcll material. In the left valve, radial costae and spines appear in the post-nepionic shell, a dense network of upraised, barbed spines being initially formed. Subsequent growth of the individual and the nature of its ornament is then strongly influenced by the nature of the substrate. There is a tendency for those individuals initially cemented within a crevice to show marked rotation of the hinge-line of up to 50°. Thus in the specimen illustrated in Figure 3A the hinge-line of the pectiniform stage is parallel to the present posterodorsal edge of the cardinal area, forming an angle of 36° with the mature stage hinge-line. Such rotations represent attempts by individuals to obtain sufficient space for opening and closing of the valves, and is similar to the ventral ward migration of the hinge-line described for Hinnites multirugosus by Yonge (1951). The shell at this point is longer than high, but thereafter the dimensions change and the height becomes the greater dimension. Phenotypic variation is overstamped by a general tendency for shells to follow in sequence the retrocrescent-infra crescent- procrescent growth directions common in cemented Pectin acea (terminology after Newell and Boyd, 1970). True xenomorphic growth sensu Stenzel, Krause and Twining (1957) is not normally seen in Spondylus american LIS. The ontogenetic development of the ornament, whilst highly variable, appears to conform to a general pattern. In the right valve the ornament is mainly foliaceous, with some marginal spine development, the relative proportions of each type depending upon the size of the area of attachment and the holdfasts available on the substrate. Cementation is primarily effected by the foliaceous growth lamellae, the spines acting as additional attachment mechanisms, as well as fulfilling their primary protective role. 574 Bulletin ot Marine Science [24(3) In most cases the attachment area is large (about one-half to two-thirds of the surface area of the attached valve) and posteriorly placed, leaving only the anterodorsal and anteroventral marginal areas as sites for spine formation. Only occasionally does the left valve show a sharply defined nepionic stage (Fig. 3B). Following this initial smooth phase, a thick mat of hair- like, barbed, solid spines, many divergent at a high angle to the shell surface (especially in the auricular regions), is developed to a valve height of about 10-15 mm (Figs. 4A-C). In this second phase, which may correspond to the neanic stage of Hyatt (1896), the spines resolve themselves into a) primary, erect to sub-erect, pointed spines, barbed on two sides along their whole length, grooved on the underside (Fig. 3G) and lying along the primary costae, and b) secondary spines, which are small, barbed, bent towards the ventral margin (Figs. 3F, 4F) and lie along barely visible intercalated costae arising by implantation. The third phase of spine development is characterized by the gradual appearance of large, scattered, sub-erect spines diverging at about 45° from the primary costae. The separation of this ephebic (?) phase from the previous one is often marked by a fairly prominent growth line. These large primary spines are solid and somewhat flattened in profile, with a longitudinal groove on the underside: their extremities form either a three- pronged point (Figs. 3F, 4D) or are splayed out into a spatula-shaped process (Figs. 3F, 4E,F). While regular primary and secondary spines continue to form with growth, those formed in the early stages of spine development are gradually worn down and almost removed in the abraded umbonal area.

OCCURRENCE OF Spondylus americanus ON BERMUDA PLATFORM

General Remarks.-The location and setting of the Bermuda Platform have been described by several authors and for recent detailed accounts of the physiography, oceanography and meteorology of the area the reader is referred to Upchurch (1970), Garrett et al. (1971), and Stephenson and Stephenson (1972). Basically the Bermuda Islands, composed mainly of calcareous aeolianites, lie on the south-eastern side of the Bermuda Plat- form, which is physiographically an atoll atop a volcanic edifice. A definite correlation between the elliptical shape of the Platform and an underlying volcanic cone of similar shape has not been established, however. Because

FIGURE 2. Map of the Bermuda Platform, showing general physiography, collecting and sediment sample localities. 1974] Logan: Morphology and Life Habits of Spondylus americanus 575

~ ~< ~ · ... ---, ~ .. , ] . . .: , ,, .. ~ ~t· , , ~• e0 ,, , e •• I , ,, t ~ .< '. l , ~ ; .. . \, ~ i e ..•\, ~ .g .l; l! ~'-' , ..•.•. _---\ .. (-j .•• \ .... ,., .•. \, ~ .. \ , , .. 0 ~~ I \ , / , I \. \.--ir'E , "- \ , ~/ ..•_-~ ~', 'e 'g0, ,- -) -' , r' - \ I , , I I I I I , ,, ,, ,, .. ,, .~ \, \ \ \ I ,, , , I, I \ (, I \ \ ,, \ , I \ \ ,, )

I .•. ; \ I , I I I \ \ \ \ \ \ I \ \ \ \, I -\/1 I \ \, ,, , "- , ,, ", "- , , \ " "- \ '-\ ' '- , / " , ,.I / / / .•..------"--//

z " 576 Bulletin of Marine Science [24(3) of its northerly latitude (32 ON), conditions for coral reef growth on the Platform are marginal and the diversity of coral taxa is thus much lower than that of the Caribbean area. Living coral and/or algal-gastropod reefs lie close to the islands on the south shore (Stanley and Swift, 1967) and elsewhere form an elongate arc of reefal shoals marginal about a central shallow lagoon (Fig. 2). In general the living reefs form only a veneer on buried Pleistocene aeolianites, whose relict topography appears to control the distribution and orientation of reef masses. The Bermuda reefs may thus be termed "reef-coral communities" following Wainwright's (1965, p. 42) definition of a reef-coral community as an assemblage of living corals or associated organisms "growing on a substrate other than that of their own recent production in shallow, tropical seas." Spondylus americanus is a common member of the Caribbean marine faunal province and has been recorded from a variety of localities (Perry and Schwengel, 1955; Olsson and McGinty, 1958; Warmke and Abbott, 1962; Storr, 1964). In Bermuda the species is ubiquitous throughout the platform in environments ranging from shallow enclosed or semi- enclosed bays (e.g. Harrington Sound, Castle Harbor) to lagoonal patch reefs (e.g. Three Hill Shoals) and open-ocean reefs (e.g. Ledge Flats, south shore reefs). In terms of Upchurch's seven biotopes (1970) it is present in the reef-front terrace biotope, the north reef biotope, the central and south reef biotope and the nearshore sandy substrate biotope. In all of these biotopes its distribution is essentially controlled by the availability of a suitably firm, creviced, coral-encrusted substrate for cementation. Study of growth form in collections from localities on the Platform representing these biotopes, however, has failed to reveal any significant relationship between form and environmental conditions. Indeed the bewildering variety in growth forms, imposed mainly by the substrate, has precluded any possibility of population analysis by conventional biometric methods. S. american us is less abundant on the south shore reefs, where coral growth is not so prolific (and where crevices and cavities are therefore more scarce) and where wave action is particularly intense for most of the year. The species is totally absent from Walsingham Pond, a land- locked marine pond of normal salinity with underground connections to Castle Harbor. A molluscan faunal list for the Pond prepared by Gould (1968) indicated the infrequent presence of the cementing bivalve Chama macerophylla on the steep limestone walls of the Pond but not Spondylus and I have also failed to observe it at this locality. In view of its common occurrence in Castle Harbor its absence from the walls of the pond is somewhat puzzling, unless it can be correlated with either the prolific sponge growth on the walls (de Laubenfels, 1950) or the absence of 1974] Logan: Morphology and Life Habits of Spondylus americanus 577 corals (and therefore the crevice habitat) from the pond. In this connection one should note that the Western Indian Ocean species Spondylus aurantius and S. hystrix were recorded by Taylor (1971) only from coral substrates (where they were cemented to branches or undersides of massive corals), and were absent from non-coralline hard substrates, although Ostrea and Chama were present on both types of substrate. In terms of depth Spondylus americanus ranges from the intertidal zone, as at Somerset Bridge and Harrington Sound, to the limits of active coral reef growth (about 20 m in most areas of the Platform).

Life Habits.-Five main modes of life of S. american us have been observed (Fig. 6): 1) Cemented to the exposed, steep face of coral reef masses or coral encrusted aeolianite surfaces (Fig. 5A). In this position the plane of commissure of the valves is usually almost parallel with the steep reef face substrate and the curved spines of the upper valve project outwards towards possible predators. Spondylus is often found cemented between corals but is rarely found adhering to the upper surface of living colonies, presumably because of the carnivorous habits of the polps towards larvae. In most cases encrustation of the upper valve and hinge area by a variety of epibionts (mostly serpulid polychaetes, vermetid gastropods, ectoproct bryozoans, sponges, bivalves [particularly chamids, Anomia, other Spon- dylus], algae and encrusting foraminifera) is heavy (Fig. 5B) and the spondylids are barely visible. A detailed search of a 23 m X 23 m study area on a patch reef in Three Hill Shoals, North Lagoon revealed only 13 exposed spondylids (yielding an average density of 1/40 m2) so open reef dwellers are by no means abundant. However, on coral encrusted aeolianite blocks within the shallow zone (Neumann, 1965) of Harrington Sound, quadrat densities of 2-3/m2 were recorded. 2) Attached to the roof and walls of crevices and cavities in the reef, where it forms part of the cryptofauna. The reef-cavity habitat in Bermuda, along with its associated flora and fauna, has been described in detail by Garrett et al. (1971) who list S. americanus as a member of both the "open" cavity-wall community and the "gloomy" cavity-wall community, especially the latter. Scoffin (1972) has examined the internal structure of the upper 2 meters of blocks of reef rock from North Lagoon patch reefs and notes the frequent occurrence of Spondylus on the cavity walls within the primary framework. My own observations support the contention that the cryptic habit is probably the commonest mode of occurrence of Spondylus on the Bermuda Platform. Although such environments are very difficult to sample quantitatively, quadrat measurements indicated average densities of living Spondylus of 1/m2 within the Three Hill Shoals study area mentioned above. 578 Bulletin of Marine Science [24(3) 3) Cemented to the lee side (underside) of the foliaceous hat coral Agaricia tragilis (Fig. 3A) where it again forms part of the cryptofauna. This coral is common in hollowed out, shaded areas of the reef, as well as in cavities, and ranges downwards in depth from just below the intertidal zone to the limit of active coral growth. Although often found attached to the upper surface of dead colonies of Agaricia, it is unlikely that spondylids ever occur cemented to the upper surface of living fronds of this coral. However, they are not uncommon on the undersides of living specimens where the ridged surface provides a moderately creviced, yet protected base for attachment in shaded areas of the reef. Faunal associates include the encrusting foraminiferan Homotrema rubrum, the diminutive articulate brachiopod Argyrotheca bermudana, ectoproct bryozoans and coralline algae. 4) Occasionally, immature living specimens of S. americanus are found domiciled within an empty, upturned, concave valve, usually of earlier- generation Spondylus, in sand channels and shell beds. Most will not survive the vicissitudes of such an existence, where turbidity is often high and valves are in danger of being overturned by currents. Moreover, growth is often constrained by the limits of the shell's dimensions, while the pressure of other individuals in the same abandoned valve may eventually seriously interfere with the opening and closing of the valves (Fig. 3C). 5) Lying free in sand channels or sand pockets at the base of reefal masses, having been dislodged from the cemented habit by storms or predators or by a weakening of the base of the coral colony, if it is so attached, by destructive biological agents such as boring sponges and bivalves. Such sand-dwelling spondylids are by no means uncommon, although it is not known how long they can survive in such a situation. Again the main threat to survival is turbulence and high turbidity during storms.

FUNCTIONAL MORPHOLOGY OF THE SPONDYLID SHELL The functional morphology of cemented epifaunal bivalves was discussed in some detail by Kauffman (1969, p. N153-159) and many of his generalized remarks on this group are applicable to the form of the spondylid shell. Thus the adaptive function of the thick shell of spondylids is undoubtedly related to the high energy conditions in which many of them live. (It should be noted, however, that those spondylids which inhabit the lower energy crevice and cavity habitats within the reefs still retain the thick shell, suggesting that it may have more than one useful function.) Also, the presence of an elevated feeding margin and a convex upper valve presumably allows the bivalve to function without undue difficulty in areas of heavy sedimentation. Furthermore, it is reasonable to assume, as Kauffman suggests, that the upper valve should paradig- 1974] Logan: Morphology and Life Habits of Spondylus americanus 579 matically be as small and light as possible to overcome the force of gravity in opening the valves, bearing in mind the immobile state of the fixed valve and the tendency for encrustation of the upper valve to further increase its weight. However, in at least one group of spondylids, those which inhabit the roofs of reef cavities, the smaller valve hangs downwards and thus the force of gravity is utilized in the opening of the valves, although, of course, it again becomes a problem when closure is necessary. The paradigmatic approach to functional analysis, first applied to bivalve shell ornament by Carter (1967), can be used to interpret the function of the various spine types already described for Spondylus americanus. Assuming there is some function to these structures (see discussion of non-functionality in Carter, 1967, p. 60; Kauffman, 1969, p. N139), we can list the following possibilities, not necessarily in order of importance: 1. The spines act as supports for sensory mantle tissue, functioning as "mantle outposts" to give early warning of approaching danger. 2. The spines serve a camouflagic function, in that they break up the distinctive outline of the shell and allow algal growth to coat the spines, so disguising the shell. 3. The spines discourage epibionts from settling on the shell. 4. The spines act as defence mechanisms for vulnerable soft parts and function in the manner of porcupine quills to keep would-be predators at bay. 5. The spines aid in attachment of the valve to the substrate. 6. The spines stabilize the shell on a shifting substrate and keep the feeding margin raised clear of the sediment. In evaluating these possible functions we can at once, because of the type of substrate to which S. americanus is normally attached and its cementing habit, reject the last possibility, although it has been invoked for the sediment-dwelling Cretaceous Spondylus spinosus by Carter (1972). We may also add that even though some of the peripheral spines of the attached right valve may help reinforce the foliaceous lamellae responsible for cementation, they do not act in a rhizoid fashion, while the spines of the upper valve are not normally in contact with the substrate. We may therefore reject the fifth possibility also. We can evaluate the other possibilities as follows: 1. The spines as sensory mantle outposts. Rudwick (1965) has invoked this function for spines in brachiopods such as the Jurassic Acanthothiris, assuming that the attenuated outer lobe of the mantle tissue within the 580 Bulletin of Marine Science [24(3)

FIGURE 3. Spondylus american us Hermann (all examples from Three Hill Shoals patch reef, unless otherwise stated). A. Right valve, showing attachment scar (striated from attachment to Agaricia), foliaceous lamellae, smooth nepionic stage with byssal notch, and ontogenetic rotation of hinge-line, X 2. B. Left valve, nepionic stage, X 7. C. Two juveniles within empty earlier- 1974] Logan: Morphology and Life Habits of Spondylus americanus 581 tubular spine of this form (and responsible for its secretion) retains communication with the inner sensory lobe. As Carter (1967) has pointed out, paradigmatically a spine primarily serving this function should have an expanded tip, in order that as much of the mantle edge as possible be exposed to the external environment. Some of the tips of the larger peripheral spines in Spondylus (Fig. 3F; 4D-F) do have this shape; however, they do not carry sensory middle mantle tissue in the specimens I have examined, although there is some connection between the secretory mantle tissue beneath the spine and the sensory mantle fold. I think it therefore likely that the primary function of these spines with an expanded tip is not a sensory one, although they undoubtedly perform this function in a secondary capacity. 2. The spines as camouflage. The typical Bermudian S. americanus usually has a dense cover of calcareous and non-calcareous algae on the upper valve surface and spines (Fig. 5B) and this tends to conceal the bivalve very effectively against its background. This camouflagic role is regarded as an important secondary function of both the primary and secondary spines, in that they come close to the paradigm for such a function; that is, they are divergent, upraised, barbed, flattened and widely distributed over and beyond the whole shell surface, acting as a structural framework for marine flora, particularly the lightly-calcified, articulated-segmented red alga such as Amphiroa, whose dense coating additionally acts as a trap for sediment particles. Particularly suitable for the attachment of algae and sediment is the thick mat of hair-like barbed spines typical of the neanic stage in the left valve of S. americanus. Grant (1966) has postulated a camouflagic and protective function for similar spines on the brachial valve of the Late Paleozoic productoid brachiopod Waagenoconcha. 3. The spines discourage epibiontic settlement. Unduly heavy settlement of epibionts may have deleterious effects on the individual spondylid by increasing the weight of the upper valve. In addition some epibionts bore into the shell and may eventually cause the death of the bivalve. The dense network of vertical, pointed spines of several orders, reinforced by stinging pedicellaria, seen in many of the regular sea-urchins, approaches most closely the paradigm for this function. The larger primary spines of Spondylus are too widely spaced and tangentially-inclined to deter any

~ generation spondylid valve, sand channel, X 1. D. Constructive epibionts within a relatively fresh left valve, shell bed, X %. E. Clionid-infested left valve, Ferry Reach patch reef, X l;j. F. Primary and secondary spines, X 9. G. Enlargement of pointed primary spine, X 8. 582 Bulletin of Marine Science [24(3)

FIGURE 4. Spondylus americanus Hermann (all examples from Three Hill Shoals patch reef, unless otherwise stated). A-C. Left valves of two juveniles, showing spine development, X 2. D-F. Spine development in two mature left valves (note juvenile Spondylus on spine in E-F), X 1. G. Grazed specimen, Nonsuch Island, Castle Harbor, X :y:;. 1974] Logan: Morphology and Life Habits of Spondylus americanus 583 but the largest epibionts; thus common adherents to the spines themselves include juvenile Ostrea frons, Chama macerophylla and Spondylus americanus (Figs. 4E,F). However the smaller, pointed, more erect primary spines and the closely-spaced network of barbed secondary spines may serve to discourage settlement of small epibionts such as boring gastropods, although the secondary spine extremities are recurved ventrally (Fig. 3F) and arc probably not a very effective deterrent. 4. The spines protect vulnerable soft parts, such as the mantle edge, from possible predators. The long, curved, ventrally-directed, barbed, primary spines covering the upper valve and extending, in some cases, beyond the valve margins, may function primarily to protect the exposed mantle edge. Many of the marginal spines have a tri-pointed extremity; in addition the primary spines are extremely strong and rigid. Carter (1967, p. 68), believes that spines fulfilling a defensive role in bivalves should "a) guard the most vulnerable part of the animal; b) be as long as possible com- mensurate with their being sufficiently strong; c) taper to a sharp point; and d) be so oriented as to face the direction of approach of expected predators." Most of the primary spines of S. american us appear to fulfill these conditions and closely approximate the paradigm for such a protective function. In conclusion, it is postulated that the main function of the larger primary spines is to protect the mantle edge from predators and, as a secondary function, to act as a framework for camouflagic algal growth. These spines are also sensory inasmuch as they contain outer mantle fold tissue in communication with sensory middle mantle fold material. The smaller pointed primary spines probably function as deterrents to epifaunal settlement. The dense network of recurved secondary spines between the primary spines may be a non-functional (or vestigial) ontogenetic feature or possibly serve to stabilize algal growth or discourage settlement of small epibionts. It is interesting to speculate on the nature of possible predators of S. american us. In Bermuda asteroids and carnivorous gastropods are uncommon. Boring bivalves are common but usually tunnel into the attached valve, and rarely threaten the existence of the individual. Carter (1968) has discussed predation in bivalves and lists a number of different groups responsible; apart from the occasional octopus, only fish are believed to pose any threat to the spondylids in Bermuda. Extensive grazing by parrot fish (Scaridae) on coral and algae has been recorded in Bermuda by Bardach (1959), Gygi (1969) and Stephenson and Stephenson (1972). Gygi (1969), reporting on the feeding habits of the parrot fish Sparisoma viride, observed the ingestion of soft algae (blue-green and green), hard calcareous algae (red) and living coral. Parrot fish are omnivorous but 584 Bulletin of Marine Science [24(3) mainly herbivorous and have been observed by the author grazing algae from the exposed valves of S. americanus and surrounding substrate at the south end of Nonsuch Island, east side of Castle Harbor. During the grazing process spines are often accidently removed and spondylids and chamids in this region appear smooth (Fig. 4G). Wrasses (Labridae) are common in Bermuda and are carnivorous. According to Bardach (1959), they feed mostly on molluscs, although it is not known whether Spondylus is included in their diet. At any rate, fish are certainly known to feed on exposed mantle tissue and Stasek (1965) reports such a case for Yridacna from Fanning Island in the Pacific. Bakus (1964, 1966) has presented the interesting suggestion that grazing and carnivorous fishes may have acted as agents of natural selection in coral reefs, resulting in the gradual development of essentially cryptic zone invertebrate faunas. He has further suggested that the evolution of protective habits and mechanisms in benthic reef organisms may have evolved in direct response to grazing and predation over a long period of time. Such selection pressure, if it existed, could conceivably have contributed to the cryptic habit and formidable spine development of many present-day reef spondylids. From the evidence of the fossil record, it would certainly appear that maximum development of spines in the spondylid group seems to have characterized essentially those reef-dwelling forms. Although the Spondylidae extend no further back than the Early Jurassic, probable ancestors of the group are well represented in the Late Paleozoic and Newell and Boyd (1970) note that spinosity is more prevalent in Permian reef-dwelling (or near reef-dwelling) pseudomonotids, aviculopectinids and terquemids than in Carboniferous or Triassic non- reef representatives.

TAPHONOMY The term "taphonomy" refers to the immediate post-mortem period between death and final entombment of the skeletal remains in the surrounding sediment. No detailed observations have been made on the taphonomy of Spondylus americanus; however, a few remarks on the main taphonomic processes responsible for the breakdown of the shell are appended here and summarized diagrammatically in Figure 6. Death, from whatever cause, is regarded as beginning when the adductor muscle is no longer able to prevent the valves from gaping freely. This appears to be the signal for fish to dart in and clean out the soft parts, an action accomplished in a matter of minutes. While unduly vigorous attack by fish may occasionally break the hinge, usually the empty valves continue to gape for some time after death (Fig. 5B). If constructive epibionts such as encrusting calcareous algae are active, then the valves are "petrified" whilst still articulated; such valves are overgrown and 1974] Logan: Morphology and Life Habits of Spondylus americanus 585

FIGURE 5. Spondylus americanus Hermann. A. Specimen attached to steep face of coral encrusted aeolianite block, 5 m, Harrington Sound. B. Gaping articulated specimen just after death, 3 m, Three Hill Shoals patch reef. C. Attached right valve soon after death, 3 m, Three Hill Shoals patch reef. D. Encrusted right valve after several months, 4 m, Harrington Sound. (All examples approximately half normal size.) 586 Bulletin of Marine Science [24(3) eventually incorporated into the reef structure in situ, before attack by destructive epibionts. More often, however, the upper valve is separated from the attached valve by predation, wave surge, or weakening of the hinge structure by decay of the ligament, chemical solution of the teeth and sockets, or breakdown by destructive organisms. The free valve may thus come to rest at the base of the reef, in a sediment pocket or sand channel. The attached valve remaining is rapidly colonized by encrusting bryozoans, algae, etc. and eventually incorporated into the reef framework (Fig. 5C, D). Those individuals dislodged from their attachment before or after death become a significant part of the localized shell beds in the sediment pockets and sand channels flanking the reef. These shell beds consist essentially of coral and mollusc rubble which is gradually encrusted by constructive epibionts and, at the same time, broken down by destructive epibionts. Shell bed constituents on Bermudian patch reefs were studied by Pohow- sky (1969) who found that most detached valves of spondylids and charnids were orientated in a concave-upwards position. Experimentally it can be shown that the upper valve of Spondylus will normally come to rest in this position after free fall from the surrounding reef face. Pohowsky also noted that encrusting forms and algae, serpulid worms, ectoproct bryozoans, vermetid gastropods and boring sponges (Fig. 3D) are the main inhabitors of the upturned spondylid valve and appear to exhibit a broad zonal distribution upon the shell surface. The role of shell surfaces as substrates for epibionts is one that deserves further and more detailed investigation. A series of painted detached valves left within a major sand channel connecting with a reef-channel in the Three Hill Shoals study area in the summer of 1971 were examined the following summer. They indicated that burial of shells is relatively rapid, and is presumably caused by the process of current scour advocated by Menard and Boucot (1951) and Johnson (1957). Most of the 70 test shells were recovered from beneath a layer of 5-8 cms of sediment, and appeared to have suffered little or no transportation in the 12-month period. Almost all had reverted to the more stable convex-upwards position, which prevails in areas of current movement; presumably early attainment of this position renders further transportation difficult (Brenchley and Newall, 1970). In contrast most of the 30 painted shells left in sediment pockets within the reef retained their original concave-upwards position, supporting the conclusions of Emery (1968) and Clifton (1971) that this is often the predominant attitude of shells in quiet water. Moreover, many were heavily encrusted, supporting the contention of Driscoll (1970) that weight gains are made during the initial year in which valves lie exposed on the substrate. Shell Breakdown.-Shells which are buried below the sediment-water inter- face undergo processes of chemical solution, organic attrition by infaunal 1974] Logan: Morphology and Life Habits of Spondylus american us 587

Open-reef dwellers Cavity dwellers Agaricia dwellers Shell-bed dwellers

------D EAT H------

BURIAL NON - BURIAL

Mechooio:ol Biological

Destruction Oe1fruclion

POTENTIAL POTENTIAL REEF FOSSILS FOSSIL SHELL SEDIMENTS BED

FIGURE 6. Diagram summarIzmg the life habits and main taphonomic processes prevailing after death in Spondylus american us. 588 Bulletin of Marine Science [24(3) TABLE 1 PERCENTAGESOF MOLLUSCAN& SPONDYLIDPARTICLETYPES FROM BERMUDA SEDIMENTSAMPLES,BASEDON 300-GRAIN COUNTS (W.S.S. = Whole Sample Summation)

Locality & No. Sieve Mollusc Spondylid (see Figure 2) Details size % % Three Hill Sediment pocket, >2mm 23 1.7 Shoals south side of 1-2 mm 13 1.5 (1) patch reef, 0.5-1 mm 10 2.2 depth 5 m W.S.S. 15 1.8 Three Hill Mid-sand channel, >2mm 12 0.3 Shoals patch reef, 1-2 mm 17 2.9 (2) depth 6 m 0.5-1 mm 8 2.1 W.S.S. 12 1.8

Three Hill Mid-slope reef >2mm 11 0 Shoals channel, patch 1-2 mm 10 1.4 (3) reef, depth 9 m 0.5-1 mm 12 1.1 W.S.S. 11 0.8

Three Hill Lagoon floor, >2mm 29 1.3 Shoals base of patch 1-2 mm 26 4.0 (4) reef, depth 14 m 0.5-1 mm 21 2.8 W.S.S. 25 2.7

Elbow Beach Inner Shoal, >2mm 15 1.0 (5) depth 9 m 1-2 mm ]6 3.4 0.5-] mm 10 6.0 W.S.S. ]4 3.5

Elbow Beach Outer Shoal, >2mm ]5 2.1 (6) depth 11 m 1-2 mm ]2 2.0 0.5 mm 12 5.0 W.S.S. 13 3.1

Warwick Long Inner Shoal, >2mm 21 2.0 Beach depth 9 m 1-2 mm 20 4.0 (7) 0.5-1 mm 17 8.3 W.S.S. 19 4.7

Warwick Long Outer Shoal, >2mm 22 2.2 Beach depth 11 m 1-2 mm 22 12.0 (8) 0.5-1 mm ]9 7.1 W.S.S. 21 8.0

North Ledge Sand channel, >2mm 44 0 Flats patch reef, 1-2 mm 12 1.0 (9) depth 9 m 0.5-1 mm 9 1.1 W.S.S. 22 1.0 1974] Logan: Morphology and Life Habits of Spondylus americanus 589 TABLE 1 (Continued)

Locality & No. Sieve Mollusc Spondylid (see Figure 2) Details size % % North Rock Sand channel, >2mm 18 7.4 (10) depth 9 m 1-2 mm 23 7.1 0.5-1 mm 18 12.0 W.S.S. 20 9.3

St. David's Sand channel, >2mm 37 0 Head depth 12 m I-201m 23 1.7 (11 ) 0.5-1 0101 12 0.8 W.S.S. 24 0.8

Castle Depth 4 01 >2mm 13 0 Harbor 1-2 mm 14 0 (12) 0.5-1 mm 12 2.2 W.S.S. 13 0.7

Castle Base of pin- >2mm 23 2.3 Harbor nacle reef, 1-2 mm 11 1.0 (13 ) depth 10 m 0.5-1 mm 10 2.0 W.S.S. 15 1.7

Castle Outer Shoal, >2mm 23 2.3 Harbor depth 11 m 1-2 mOl 10 0.8 (14) 0.5-1 mm 6 1.4 W.S.S. 13 1.8

Harrington Abbott's Cliff, >2mm 66 12.1 Sound sandy zone, 1-2 mm 30 12.6 (15) depth 5 m 0.5-1 mm 15 5.0 W.S.S. 40 10.0

Harrington Patton's Point, >2mm 64 12.3 Sound sandy zone, 1-2 mm 25 4.6 (16) depth 6 m 0.5-1 mm 12 3.6 W.S.S. 36 7.3 organisms and corrosion and solution following bacterial decomposition of soft parts (Revelle & Fairbridge, 1957; Fairbridge, 1967). This stage has been termed "syndiagenesis" by Bissell (1959) and precedes compac- tion and cementation of the sediments. Shells which are not immediately buried are subject to either mechanical, biological or chemical destruction. Mainly on the basis of tumbling barrel experiments on the tests of shelly organisms and comparison of the sediment yield with naturally-occurring sediments, Upchurch (1970) has suggested that mechanical destruction is the dominant process responsible 590 Bulletin of Marine Science [24(3) for sediment formation on the Bermuda Platform, aided by weakening of the shell architecture by biological destruction, with chemical solution relatively unimportant. The role of organisms in shell breakdown has been discussed by many authors, including Ginsburg (1957), Y onge (1963), James (1970) and Upchurch (1970) and will not be elaborated upon here. Suffice to say that endolithic algae, sponges, worms and boring bivalves act primarily as weakening agents of the fairly resistant spondylid shells and that coarse skeletal fragments are further triturated mainly by echinoderms and gastropods. Of particular importance in biological destruction are clionid sponges (Goreau and Hartman, 1963; Neumann, 1966), which may infect spondylids before death (Fig. SA) and continue to produce extensive galleries in the shell after death (Fig. 3E). The relative amounts of spondylid detritus in the coarser fractions of sediment samples taken from a variety of environments on the Platform are shown in Table 1. From these analyses Spondylus is seen to be a relatively minor contributor to the sediment (usually less than 5 % ) . Abnormally high values in Harrington Sound might suggest a general relationship with standing crop but because of the relatively slow rate of breakdown of shells, plus the absence of data on the life expectancy of this form, such conclusions, as Turney and Perkins (1972) have remarked, are higWy speculative.

ACKNOWLEDGMENTS

I would like to thank G. R. Webb for diving assistance and the Bermuda Biological Station for facilities. Dr. M. L. H. Thomas of University of New Brunswick kindly read and criticized the manuscript. The work was carried out during July, 1971 and was supported by NRC Grant A 4331.

REFERENCES BAKUS, G. J. 1964. The effects of fish-grazing on invertebrate evolution in shallow tropical waters. Allan Hancock Foundation Occ. Papers, No. 27: 29 pages. ]966. Some relationships of fishes to benthic organisms on coral reefs. Nature, 210: 280-284. BARDAcH, J. E. 1959. The summer standing crop of fish on a shallow Bermuda reef. Limno!. Oceanogr. 4(1): 77-85. BISSELL, H. J. 1959. Silica in sediments of the Upper Paleozoic of the Cordilleran area. In Ireland, H. A. (Editor), Silica in Sediments, S.E.P.M. Sp. Pub!. 7: 150-185. B0GGILD, O. B. 1930. The shell structure of the molluscs. Mem. Acad. Roy. Sci. Lett. Dan. Ninth Series, II (2): 235-325, 15 pIs. Copenhagen. 1974] Logan: Morphology and Life Habits of Spondylus americanus 591

BRENCHLEY, P. J. AND G. NEWALL 1970. Flume experiments on the orientation and transport of models and shell valves. Palaeogeography, Palaeoclimatol., Palaeoeco\., 7: 185-220. BRETSKY, S. S. ] 967. Environmental factors influencing the distribution of Barbatia domin- gensis (Mollusca, Bivalvia) on the Bermuda Platform. Postilla, no. 108: 14 pages. BULLIVANT, J. S. 1962. Direct observation of spawning in the Blacklip Pearl Shell Oyster (Pinetada margaritifera) and the Thorny Oyster (Spondylus sp.). Nature, 193: 700-701. CARTER, R. M. 1967. The shell ornament of Hysterocollcha and Hecuba (Bivalvia): a test case for inferential functional morphology. Veliger, 10(1): 59-71, 3 pIs. 1968. On the biology and palaeontology of some predators of bivalved mollusca. Palaeogeography, Palaeoclimato\., Palaeoeco\., 4: 29-65, 2 pIs. 1972. Adaptations of British Chalk Bivalvia. J. Paleontol., 46(3): 325-340, 3 pis. CLIFTON, H. E. 1971. Orientation of empty pelecypod shells and shell fragments in quiet water. J. Sed. Petrol., 41 (3): 671-682. COMFORT, A. 1951. The pigmentation of molluscan shells. BioI. Reviews, 26: 285-301. DAKIN, W. J. 1928a. The anatomy and phylogeny of Spondylus, with a particular reference to the lamellibranch nervous system. Proc. Roy. Soc. London, Ser. B., ]03: 337-355. 1928b. The eyes of Pecten, Spondylus, Amussium and allied lamellibranchs, with a short discussion on their evolution. Trans. Roy. Soc. London, Ser. B., 103: 355-365. DRISCOLL, E. G. 1970. Selective bivalve shell destruction in marine environments, a field study. J. Sed. Petrology, 40(3): 898-905. EMERY, K. O. 1968. Positions of empty pelecypod valves on the continental shelf. J. Sed. Petrology, 38(4): 1264-1269. FAIRBRIDGE, R. W. 1967. Phases of diagenesis and authigenesis. In Larsen, G. and G. V. Chilingar (Editors), Diagenesis in Sediments. Developments in Sedimentology 8, Elsevier: 19-89. GARRETT, P., D. L. SMITH, A. O. WILSON AND D. PATRIQUIN 1971. Physiography, ecology, and sediments of two Bermuda patch reefs. 1. Geo\., 79: 647-668. GINSBURG, R. N. 1957. Early diagenesis and lithification of shallow-water carbonate sediments in south Florida. In Le Blanc, R. J. and Julia G. Breeding (Editors), Regional Aspects of Carbonate Deposition, S.E.P.M. Sp. Pub\. 5: 80-100. 592 Bulletin of Marine Science [24(3)

GOREAU, T. F. AND W. D. HARTMAN 1963. Boring sponges as controlling factors in the formation and mainte- nance of coral reefs. In Mechanisms of Hard Tissue Destruction, Am. Assoc. Adv. Sci. Pub. No. 75: 25-54. GOULD, S. J. 1968. The molluscan fauna of an unusual Bermudian pond: a natural experiment in form and composition. Breviora, no. 308: 1-13. GRANT, R. E. 1966. Spine arrangement and life habits of the productoid brachiopod Waagenoconcha. J. Paleontol., 40(5): 1063-1069, 2 pis. GUTSELL, J. S. 1931. Natural history of the bay scallop. Bull. U. S. Bur. Fish., 46: 569-632. GYGI,R.A. 1969. An estimate of the erosional effect of Sparisoma viride (Bonaterre), the green parrotfish, on some Bermuda reefs. Berm. BioI. Stn. for Res., Sp. Publ. 2: 137-143. HYATT, A. 1896. Terminology proposed for description of the shell in Pelecypods. Am. Assoc. Adv. Sci., Proc., 44: 145-148. JACKSON, R. T. 1890. Phylogeny of the Pelecypod a, the Aviculidae and their allies. Boston Soc. Nat. Rist., Mem., 4: 277-400. JAMES, N. P. 1970. Role of boring organisms in the coral reefs of the Bermuda Platform. Berm. BioI. Stn. for Res., Sp. Publ. 6: 19-27, 2 pis. JOHNSON, R. B. 1957. Experiments on the burial of shells. J. Geol., 65(5): 527-535. KAUFFMAN, E. G. 1969. Form, function and evolution. In Moore, R. C. (Editor), Treatise on Invertebrate Paleontology, Pt. N., Mollusca 6, Bivalvia: N 129- 205. Geol. Soc. America and Univ. Kansas Press. LAUBENFELS, M. W. DE 1950. An ecological discussion of the sponges of Bermuda. Trans. Zool. Soc. London, 27(1): 155-201. MENARD, R. W. AND A. J. BOUCOT 1951. Experiments on the movement of shells by water. Am. J. Sci., 249: 131-151. NEUMANN, A. C. 1965. Processes of Recent carbonate sedimentation in Harrington Sound, Bermuda. Bull. Mar. Sc., 15: 988-1035. 1966. Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge, Cliona lampa. Limnol. Oceanogr., 11: 92-108. NEWELL, N. D. 1969. Classification of Bivalvia. Tn Moore, R. C. (Editor), Treatise on Invertebrate Paleontology, Pt. N., Mollusca 6, Bivalvia: N 205-224. Geol. Soc. America and Univ. Kansas Press. NEWELL, N. D. AND D. W. BOYD 1970. Oyster-like Permian Bivalvia. Bull. Amer. Mus. Nat. Rist., 143(4): 217-282, figs. 1-34, 6 tables. 1974] Logan: Morphology and Life Habits of Spondylus americanus 593

NICOL, D. 1964. Lack of shell-attached pelecypods in Arctic and Antartic waters. Nautilus, 77(3): 92-93. 1965. Ecologic implications of living pelecypods with calcareous spines. Nautilus, 78(4): 109-115. OLSSON, A. A. AND T. L. McGINTY 1958. Recent marine mollusks from the Caribbean Coast of Panama with the description of some new genera and species. Bull. Amer. Paleontol., 39( 177): 52 pages, 5 plates. OMORI, M. AND I. KOBAYASHI 1963. On the micro-canal structures found in the shell of Area navieularis Bruguiere and Spondylus barbatus Reeve. Venus, 22(3): 274-280, 2 pIs. PERRY, L. M. AND J. S. SCHWENGEL 1955. Marine shells of the western coast of Florida. Pal. Res. Inst: 198 pages, 55 pIs. POHOWSKY, R. A. 1969. Studies on the sedimentology and ecology of shell beds on Bermudian patch reefs. Berm. Bio. Stn. for Res., Sp. Publ. 2: 101-123. REVELLE, R. AND R. FAIRBRlDGE 1957. Carbonates and carbon dioxide. In Hedgpeth, J. W. (Editor), Trea- tise on Marine Ecology & Paleoecology, 1, Ecology: 239-295, Geol. Soc. Amer. Mem. 67. RUDWICK, M. J. S. 1965. Sensory spines in the Jurassic brachiopod A eanthothiris. Palae- ontology, 8(4): 604-617,4 pIs. SCOFF IN, T. P. 1972. Fossilization of Bermuda patch reefs. Science, 178: 1280-1282. STANLEY, D. J. AND D. J. P. SWIFT 1967. Bermuda's southern aeolianite reef tract. Science, 157: 677-681. STANLEY, S. M. 1970. Relation of shell form to life habits in the Bivalvia (Mollusca). Geo1. Soc. America, Mem. 125, 199 pages, 40 pls. STASEK, C. R. 1965. Behavioral adaptation of the Giant Clam Tridaena maxima to the presence of grazing fishes. Veliger, 8( 1): 29-35. STENZEL, H. B., E. K. KRAUSE AND J. T. TWINING 1957. Pelecypod a from the type locality of the Stone City Beds (Middle Eocene) of Texas. Univ. Texas, Bur. Econ. Geology, no. 5704: 237 pages, 22 pis. STEPHENSON, T. A. AND ANNE STEPHENSON 1972. Life between tidemarks on rocky shores. W. H. Freeman & Co., San Francisco. 402 pages. STORR, J. F. 1964. Ecology and oceanography of the coral-reef tract, Abaco Island, Bahamas. Geol. Soc. Amer., Sp. Pap. 79, 94 pages, 8 pis. TAYLOR, J. D. 1971. Reef associated molluscan assemblages in the Western Indian Ocean. Tn Stoddart, D. R. and Sir Maurice Yonge (Editors), Regional Variation in Indian Ocean Coral Reefs, Symp. zool. Soc. Lond., no. 28: 501-534. 594 Bulletin of Marine Science [24(3)

TAYLOR, J. D., W. J. KENNEDY AND A. HALL 1969. The shell structure and mineralogy of the Bivalvia. Introduction. Nuculacea-Trigonacea. Bull. Brit. Mus. Nat. Rist. (Zoo\.) Suppl. 3: 125 pages, 29 pis. THORSON, G. 1946. Reproduction and larval development of Danish marine bottom invertebrates. Medd. Danm. Fisk.-og Havunders., Ser. Plankton, 4: 1-523. 1966. Some factors influencing the recruitment and establishment of marine benthic communities. Netherlands Journal of Sea Research, 3(2): 267-293. TURNEY, W. J. AND R. F. PERKINS 1972. Molluscan distribution in Florida Bay. Sedimenta III, Compo Sed. Lab., U. of Miami, 37 pages. UPCHURCH, S. B. 1970. Sedimentation on the Bermuda Platform. U. S. Lake Survey, Res. Rep. 2-2: 172 pages. WAINWRIGHT, S. A. 1965. Reef communities visited by the Israel South Red Sea Expedition, 1962. Israel South Red Sea Exped. 1962 Reports No.9. Bull. Sea Fish Res. Stn. Israel, 38: 40-53. WARMKE, G. L. AND R. T. ABBOTT 1962. Caribbean Seashells. Livingston Publishing Company, Narberth, Pennsylvania, 229 pp., 44 pIs. WILSON, D. P. 1952. The influence of the nature of the substratum on the metamorphosis of the larvae of marine animals, especially the larvae of Ophelia hicornis Savigny. Ann. Inst. Oceanogr., 27: 49-156. YONGE, C. M. 1951. Studies on Pacific Coast mollusks. 3. Observations on Hinnites multirugosus (Gale). Univ. Calif. Pub\. Zool., 55: 409-420. 1963. Rock-boring organisms. In Mechanisms of Hard Tissue Destruction, Amer. Assoc. Adv. Sci., Pub. No. 75: 1-24. 1973. Functional morphology with particular reference to hinge and ligament in Spondylus and Plicatula and a discussion on relations within the superfamily Pectinacea (Mollusca: Bivalvia). Trans. Roy. Soc. London, Ser. B, 267: 173-208.