the biology and functional morphology of myochama anomioides ...

J. Moll. Stud. (2000), 66, 403–416

© The Malacological Society of London 2000

THE BIOLOGY AND FUNCTIONAL MORPHOLOGY OF MYOCHAMA ANOMIOIDES STUTCHBURY, 1830 (BIVALVIA: ANOMALODESMATA: PANDOROIDEA), WITH REFERENCE TO CEMENTATION ELIZABETH M. HARPER 1 and BRIAN MORTON 2 1

Department of Earth Sciences, Downing Street, Cambridge CB2 3EQ, UK 2 Swire Institute of Marine Science and Department of Ecology and Biodiversity, The University of Hong Kong, Hong Kong (Received 14 December 1999; accepted 4 February 2000)

ABSTRACT

INTRODUCTION

The small, exclusively Australasian, anomalodesmatan family Myochamidae comprises only two genera; the shallow-burrowing Myadora and the cementing Myochama. This paper describes the anatomy and cementing behaviour of Myochama anomioides and draws comparisons with Myadora. The anatomy of Myochama anomioides is little different from that previously described for Myadora, except that they are mirror images. Valve inequality is not reflected in the organs of the mantle cavity in either taxon. Such differences which are present, for example the reduction of the foot in Myochama, mostly relate to the adoption of a sessile habit. There are few differences in mantle folds of the cementing and non-cementing genus, except that in M. anomioides the right mantle fold, which secretes the cemented valve, is thicker and less well–developed than the left. During the cementation process, the periostracum secreted by the right fold is thinner and has a quilted appearance. Individuals of Myochama anomioides cement by their right valve once they have reached a size of 1.2–3.9 mm. They appear to have a preference for attaching to the posterior portions of a diversity of living, shallow infaunal bivalves. The pronounced stereotypic orientation they adopt suggests that these hosts are most often alive at the time of colonization and that the myochamids benefit from the relationship. The relationship, however, is not obligate. They are capable of attaching to other shelly or rock debris, but do so at a larger size, presumably when the preferred substrata are not available. The thin layer of extra-periostracal cement lacks the calcareous crystalline nature of oyster cement, instead being largely composed of organic material. This cement is presumably secreted by glands within the mantle, but these have not been identified. Indeed, the mantle lacks arenophilic glands which might have been thought a suitable candidate for supplying cement.

Cementation by one valve to a hard substratum is often seen as the culmination of the epifaunal habit in bivalves (Yonge, 1979). The principal exponents, the oysters and extinct rudists, have been amongst the most successful members of the class. Cementation is known to have evolved independently in a large number of bivalve taxa (Yonge, 1979; Harper, 1991a,b, 1992) but has arisen more often in some major bivalve clades than in others. Most cementing clades belong to either the pteriomorphs, including the oysters, dimyids, spondylids and various pectinids, or the heteroconchs, including the rudists and chamids, and two small clades within the anomalodesmatans i.e., the Cleidothaeridae and Myochamidae. In the freshwater bivalves, cementation has evolved within the Etheriidae (itself probably a polyphyletic assemblage (Bogan & Hoeh, in press)) and has recently been recognised in a newly described Indonesian species of corbiculid (Posostrea anomioides) (Bogan & Bouchet, 1999). There are no records of cementing protobranchs, arcoids, mytiloids or lucinoids. The mechanism of cementation and its evolution have been studied most intensively in the pteriomorphs (Cranfield, 1973a,b,c, 1974; Yonge, 1979; Harper, 1992, 1997), largely because of the abundance and economic importance of oysters. In most Pteriomorpha, the habit appears to have evolved in the Late Palaeozoic or Early Mesozoic (with the exception of several pectinid cementers, e.g. Hinnites, which have Cenozoic origins) (Harper, 1991a). It is apparent that these cementers evolved directly from pleurothetic epibyssate stock and all pass through a byssate phase early in their ontogenies. Adult attachment is achieved by a calcareous crystalline

Corresponding author: e-mail: [email protected]

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cement (Harper 1992, 1997). There is a marked temporal coincidence between the multiple evolution of the cemented habit in a number of taxa during the early Mesozoic and the onset of increased predation pressure during the Mesozoic Marine Revolution (Vermeij, 1987) and Harper (1991a) has demonstrated experimentally the defensive value of cementation over epibyssate attachment. In order to understand further the multiple evolution of the cemented habit within the Bivalvia, it is of interest to examine cementing behaviour in other clades, even though these may be smaller and contain less well-known taxa, to provide comparisons with the pteriomorphs. Do they cement in the same manner and were different selection pressures involved in the evolution of the habit? This paper focuses on the evolution of cementation in the anomalodesmatan family Myochamidae. This is a small family of the Pandoroidea comprising only two genera (both living and fossil), Myochama Stutchbury, 1830 and Myadora Gray, 1840, of which only the former cements, by the right valve, typically to the posterior region of large infaunal bivalves (Yonge & Morton, 1980; Prezant, 1998). By contrast, individuals of Myadora are actively burrowers and Morton (1977) recorded Myadora striata (Quoy & Gaimard, 1835) lying on its left valve within the sediment. [Tevesz (1975) reported upon an individual of Myadora cf. pandoriformis Stutchbury burrowing with its right valve downwards.] Myadora occurs throughout the southern Pacific but Myochama is restricted to southeastern Australia (including Tasmania) and New Zealand (Prezant, 1998). The family has been little studied: Tevesz (1975) and Morton (1977) described the functional morphology of Myadora, whilst apart from inclusion in a study of pandoroidean ligaments by Yonge & Morton (1980), Myochama has been little mentioned in the literature since the brief description by Hancock (1853). Cementation in the Myochamidae has arisen much more recently than in the majority of pteriomorphs, Myochama being first recorded from the Upper Oligocene (Beu & Maxwell, 1990). It appears (see Discussion) to have arisen from the infaunal abyssate Myadora, a situation rather different from that of the pteriomorphs where cementation arose from epibyssate taxa. The relative recency of the acquisition of the cemented habit in the Myochamidae, however, should allow a comparison to be made between the anatomies of its two constituent genera and,

thereby, reveal the direct effects of cementation on the body plan. Although cementation in the Myochamidae is restricted to a single genus, the habit has also evolved in other members of the Anomalodesmata. The cementing Cleidothaeridae, another small, exclusively Australasian family also belonging to the Pandoroidea, has been studied by Morton (1974). Species of this family attach by the right valve to open rock surfaces both intertidally and in the shallow sub-tidal. Members of the enigmatic Clavagellidae attach, by either one or two valves, to their adventitious tubes (Morton, 1984a,b), although they are not generally considered as cementing bivalves as they are not ecologically equivalent. The manner of attachment of cleidothaerids and clavagellids has never been investigated in detail, however, it was suggested that the former might attach by way of a ‘sticky’ outer periostracal layer (Morton, 1974) and that the latter achieve valve adhesion using secretions from arenophilic mantle glands around the siphons (Morton, 1984a). The latter is an interesting suggestion because these glands have been reported upon in other anomalodesmatan bivalves, for example, species of the Lyonsiidae, Periplomatidae and Parilimyidae, where their secretions are involved in the fixation of sand grains and other debris to the outer surface of the shell (Prezant, 1979; Morton, 1987). It is then at least a plausible hypothesis that other anomalodesmatans, i.e. cleidothaerids and myochamids, might also use similar secretions to cement themselves to hard substrata. This study had two specific aims: (i), to investigate the cemented habit of Myochama, and (ii) to compare the anatomy of Myochama with that described for Myadora striata by Morton (1977) in order to identify significant differences which either have pre-adapted Myochama for cemented habit or have been direct consequences of its evolution.

MATERIALS AND METHODS Specimens of Recent and fossil Myochama were studied in the collections of the Australian Museum, Sydney (AM), National Museum of Victoria, Melbourne (NMV) and the Natural History Museum (London) (NHM). A census of individuals of Myochama anomioides Stutchbury, 1830 in the AM collections was used to determine the identity of the substrata to which they attach. All available material was studied by first examining the myochamid collections and then the collections of the hosts. For those animals attached to the external surfaces of other

CEMENTATION IN MYOCHAMA ANOMIOIDES bivalves, the relative orientations of each of the myochamids relative to its host were measured by determining the angle between the dorso-ventral axes of the latter and the former (see Fig. 1A). The abrupt change in shell ornamentation at the onset of cementation allowed measurements of the valve height at attachment to be made for a number of individual Myochama anomioides. This was possible for individuals that had either been detached from their substrata or had the dorsal part of the unattached valve neither abraded nor overgrown by epibionts. Measurements were made using vernier calipers to the nearest 0.1 mm. Shell microstructure and surface features of Myochama anomioides were studied by SEM (JEOL 820). Elemental analysis of specific areas was undertaken using x-ray microanalysis (Link AN 10 000 software). The manner of cementation was investigated using several M. anomioides attached to the smooth periostracum of Eucrassatella kingicola (Lamarck, 1805) (unregistered specimen (NHM) collected from Two

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Fold Bay, New South Wales). Microstructural details of both the valves and cementing regions were determined from either fractured surfaces or etched polished sections. The latter were made by setting valves in blocks of epoxy resin which were then cut along the maximum growth direction. The surfaces were then polished using a series of carborundum powders and finally etched for 25 seconds in 1% hydrochloric acid. It was also possible to inspect the cement on underside of the right valve of a specimen which had apparently once been attached to a coarse sedimentary rock. The inner surface of the periostracum was investigated at the ventral valve margins where it naturally lifts away from the shell, and by setting the outer valve surface in epoxy resin and then dissolving away the calcareous component of the shell. All preparations were air-dried except for the latter, which was critical point dried (CPD) using liquid carbon dioxide as the ambient fluid. The histological details of a single specimen of Myochama anomioides (NMV F80239), attached to a

Figure 1. Attachment of Myochama anomioides. A. An external view of the right valve of Neotrigonia margaritacea with an attached M. anomioides showing the measurement of the angle (°) taken between the dorsoventral axes of the host (a-b) and cemented symbiont (x-y). B. Rose diagram of the percentage distributions of host Neotrigonia spp., Eucrassatella spp., Glycymeris spp. and Venericardia amabilis (pooled). C. An external view of the right valve of Eucrassatella kingicola showing a specimen of M. anomioides in its preferred orientation ( 50°) and the inhalant and exhalant currents of the two bivalves.

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glycymerid, collected in 1973 from a water depth of 48 m from the Eastern Bass Strait, New South Wales, Australia, were examined. This specimen had been stored in ethanol, however, we have no information about its fixation history. The left valve and the tissues were carefully separated from the attached right valve, decalcified and sectioned transversely at 6m. Alternate slides were stained in either Ehrlich’s haematoxylin and eosin or Masson’s trichrome. Anatomical observations were made of other preserved specimens of Myochama anomioides and comparisons made with observations on Myadora striata reported upon by Morton (1977).

RESULTS Pre-attachment shell SEM micrographs of the pre-attachment shell of Myochama anomioides show that the prodissoconch, identifiable by its lack of ornament, is often missing having broken along the boundary with the dissoconch. Where present, the prodissoconch height was approximately 250 m but it was not possible to accurately determine the prodissoconch I/II boundary. The preattachment dissoconch (Fig. 2) is inequivalve, with a flat right valve. Although we suspect that prior to cementation, small M. anomioides, like most juvenile bivalves (Yonge, 1962), are held in place by a small byssus, this is not reflected by any morphological evidence in the shell. The onset of cemented attachment (at valve heights between 1.2 and 3.9 mm) is marked by a sharp change in valve morphology when both valves, the right in particular, becomes irregular losing its allomorphic ornament

Choice of substratum The results of the survey of substrata used by individuals of Myochama anomioides in the Recent collections of the Australian Museum as shown in Table 1. Of 126 individuals, the vast majority (c.89%) were attached to the external surfaces of other bivalves. Although over half of them were attached to the three genera with which they are generally associated, as noted by Cotton (1961), there is a much greater diversity of hosts. The overall impression of these data is that shallow-burrowing infaunal bivalves, in particular larger taxa, are preferred as host substrata. An analysis of the patterns of Myochama settlement on the four most recorded hosts i.e., Neotrigonia, Eucrassatella, Venericardia and Glycymeris revealed that there was no significant difference between the numbers of individuals which had settled on the right and left valves. Virtually all individuals were attached to the posterior half of the valves, usually close to the posterior margin, which had presumably been exposed at the substratum-water interface. Fig. 1B shows the orientation of 99 individuals of M. anomioides recorded relative to their host’s shells. Most adopted a position such that the dorso-ventral axis of the shell was at 40–60° to that of the host (regardless of the taxon). Obviously, the host need not necessarily have been alive at the time of myochamid settlement but this pronounced stereotypy of positioning and the relative paucity of individuals attached to the inside of host valves, suggests that the majority were. This preferred positioning directs the myochamid’s siphons Table 1. Results of the census of the identity of the substratum utilised by the 124 individuals of attached Myochama anomioides in the collections of the Australian Museum. Substrata used

Figure 2. Scanning electron micrograph of the umbo of the left (unattached) valve of Myochama anomioides showing the pre-attachment part of the valve. Onset of attachment is marked by valve distortion, shown by the arrow. Scale bar 1 mm.

Neotrigonia spp. Venericardia amabilis (Deshayes) Glycymeris spp. Eucrassatella spp. Tawera gallinula (Lamarck) Myadora brevis (Stutchbury) Circe scripta (Linnaeus) Tucetona broadfooti (Iredale) Dosinia juvenilis (Gmelin) Fragum retusum (Linnaeus) Corbula tunicata (Hinds) Inanimate objects and empty valves

No. of Myochama anomioides 32 26 23 17 4 3 2 2 1 1 2 14

CEMENTATION IN MYOCHAMA ANOMIOIDES

directly towards the inhalant siphon of the host (Fig. 1C). Such an arrangement presumably ensures its siphons, like those of the host, are at the sediment/water interface and may also benefit the myochamid by enhancing its inhalant flow. Hosts were not infrequently colonised by a single myochamid, but several had multiple (up to 8) individuals attached, all with similar orientations. Crowding was often such that their margins interdigitated and, as noted by Yonge & Morton (1980) and figured by Prezant (1998, Fig. 9.14f), overgrowth of smaller by larger individuals occurred. There was also evidence of multiple generations of encrustation where later-settling individuals were attached to the interior of the right valves of earlier ones. A similar survey of fossil myochamids in the NMV collections revealed that these exhibited similar host preferences. Of 41 specimens of fossil Myochama that were examined (Oligocene to Pliocene) all were attached to the outsides of large bivalves: Eucrassatella spp. (31.7%); Glycymeris spp. (24.4%); Neotrigonia spp. (19.5%); Cucullaea spp. (17.1%), an indeterminate venerid (4.9%) and Myadora spp. (2.4%). Although exact measurements were not made, most individuals also showed an orientation towards the inhalant current of the host. A significant proportion (11%) of the AM specimens were attached to inanimate objects, i.e. empty shells and barnacles (distinguished by their attachment to the inner surfaces of their ‘host’) or rock fragments. It is possible that myochamids attached to rock may be underrepresented in collections because of the difficulty in collecting and storing this type of material and, thus, the importance of these substrata may be under-estimated. Measurements of the valve height at which cementation commenced ranged from 1.2–3.9 mm. Analysis of these data in relation to substratum type showed that those individuals attached to ‘live’ substrata did so at a smaller mean valve height of 1.7 mm (n-1 0.31; n 74), then those attached to either the insides of empty valves or to rocks which did so at a mean height of 2.9mm (n-1 0.57; n 6). Despite the small number of individuals in the latter group, the Mann-Whitney test shows that the size difference between the two groups is highly significant at above the 1% level. Post-attachment shell Post-attachment individuals of Myochama anomioides are trigonal and grossly inequivalve,

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the attached right valve being flat to slightly convex and markedly thinner than the more robust, highly concave left valve. The valves are also slightly discordant, the height of the left valve being slightly greater than that of the right. Myochama anomioides is approximately isomyarian, with a bean-shaped anterior adductor muscle scar (Fig. 3, AA) whereas the posterior (PA) is more oval. The former muscle is located ventral to the mid antero-posterior axis of the shell while the latter lies above it. There are no pedal retractor muscle scars. The thin pallial line (PL) is deeply indented from the shell margin and there is a shallow pallial sinus posteriorly (PS). The hinge plate (Fig. 3) comprises an amphidetic primary ligament located on a resilifer. The central element is the inner ligament layer (IL) (Yonge, 1976) ( fibrous layer [Waller, 1990]). Antero-dorsally and postero-dorsally of this are larger anterior (AOL) and smaller posterior (POL) outer ligament layers (Yonge, 1976) ( lamellar ligament layers [Waller, 1990]). The entire dorsal margin of the shell is also connected by what Yonge (1976) termed ‘fused’ periostracum (‘F’P) and which forms a thickened pad, or ‘secondary ligament’, above the primary one. The lithodesma (L) lies ventral to the ligament. The hinge plate of the

Figure 3. Myochama anomioides. Internal views of the shell: A. The attached right valve and B. The left valve (For abbreviations see p. 414).

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attached right valve also has a long anterior tooth (AHT) and a more robust one posteriorly (PHT). These lock under the hinge plate of the left valve, which is edentulous (Fig. 4). The structure of the ligament is shown in transverse section in Fig. 5. Left and right elements of the inner ligament layer (IL) are secreted externally by the underlying mantle (ME). They are also secreted internally by an anterior ‘tongue’ of mantle tissue (TT). The same tongue of tissue dorsally secretes the pad of ‘fused’ periostracum (‘F’P) that is contiguous with the outer layer of periostracum (OP) that overlies the shell, but, importantly, not the inner periostracal layer (IP). In its form, therefore, the ligament of Myochama anomioides is of the basic anomalodesmatan plan (Yonge & Morton,

Figure 4. Myochama anomioides. The shell as seen from the posterior aspect (For abbreviations see p. 414).

Figure 5. Myochama anomioides. A transverse section through the ligament (For abbreviations see p. 414).

1980) and it is significant that the cemented habit has not resulted in an asymmetry to its structure despite the pronounced inequivalvy. Shell microstructure Taylor, Kennedy & Hall (1973) reported that the valve microstructure of Myochama anomioides and Myadora striata were wholly aragonitic and comprised three principal layers; an outer prismatic layer and middle and inner layers of lenticular and sheet nacre, respectively. This investigation has, however, shown that the shell microstructure of M. anomioides deviates in a number of important respects from the basic anomalodesmatan pattern and that there are significant differences between the two valves. The left, unattached, valve is generally thicker and is composed almost entirely of sheet nacre. The extreme outer layer of the shell lacks the convincing prismatic microstructure commonly associated with most anomalodesmatans (Taylor et al.,1973). The external surface of this valve is bounded by a periostracal sheet up to 14m thick, although in some areas, particularly dorsally, this is reduced, presumably by abrasion. The external surface of the periostracum has a ‘ropey’ texture but this is not reflected in its internal structure which is structure-less and not obviously layered (Fig. 6D). The surface is also studded with small spikes arranged in radial rows and resemble those described for other anomalodesmatans, e.g. Thracia, Penicillus, Poromya and Laternula (Taylor et al., 1973; Aller, 1974). The inner surface of the periostracum is pitted with, irregularly-distributed, hexagonal craters, up to 10 m across, which reduce in width as they pass into the periostracum but do not completely penetrate the periostracal sheet (Fig. 6A). Critical point dried preparations of the inner surface of the periostracal sheet shows that each crater is lined with an ultra-thin film of material (0.5 m), herein considered to be the inner layer of periostracum which forms a ragged skirt around its circumference and may form wrinkled areas between craters (Fig. 6B). The distribution of the craters correspond with those of pyramidal protuberances on the external surface of the shell and which terminate at a small hexagonal boss, sometimes missing (Fig. 6C, D). Shallow saucer-shaped depressions are left in the surface of the shell in areas where the protuberances have been lost. Similar bosses on the outside of the shell have been described and illustrated for another anomalodesmatan taxon Thracia phaseolina (Lamarck) by Taylor


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Figure 6. Scanning electron micrographs of the periostracum and outer shell surface of the left (unattached) valve of Myochama anomioides. A. Inner surface of the periostracal sheet (air-dried); scale bar 100 m. B. Inner surface of the periostracal sheet (critical point dried); scale bar 10 m. C. Pyramidal protuberances on the outside of the valve, scale bar 10 m. D. Etched cross section through the periostracum (P) showing the pyramidal protuberances within the craters; scale bar 10m.

(1973) and also the palaeoheterodont Neotrigonia magaritacea (Lamarck) by Taylor et al. (1969). The latter authors have interpreted these structures as representing the initial spherulite from which the prisms in the outer shell layer subsequently grew. This is an interesting observation as Cope (1997) has suggested that the Anomalodesmata were derived from the Palaeoheterodonta. It seems probable to us that the bosses on the outside of Myochama anomioides are also the vestiges of the prismatic shell layer which has been all but lost. The appearance of the protuberances and the craters into which they fit suggest that the growth of the crystallites caused the holes in a pliable periostracal sheet rather being cast within them. The thinner, attached, right valve is also predominantly made up of sheet nacre but is bounded by a thin (10 m) layer of fine aragonite prisms (0.5 m in width), (Fig. 7). The underlying periostracum between the shell and its substratum is particularly notable. Here there is no sign of the dense homogenous outer periostracal layer, nor of the pyramidal protu-

Figure 7. Scanning electron micrograph of the detailed microstructure of the right (attached) valve of Myochama anomioides; scale bar 10 m.

berances, although the former are clearly visible over the external surface of the valve where it is not attached, i.e. dorsally and at the ventral valve margins where no cementation occurs. Rather, the sheet has a quilted appearance (Fig. 8B,C) and seems to consist of a double layer of

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thin crenulated sheets (0.5 m thick) separated by some 10–20 m and connected by cross walls. The space between the two sheets is occupied by a homogenous crystalline material, which etches back from the sheet. The calcareous nature of this infill was confirmed by x-ray micro-analysis.

Character of the cement There is a definite layer of cement between the right valves of Myochama anomioides and their substrata (Fig. 8A,B,C). It has an average thickness of around 20 m but which accumulates in topographic hollows within the substratum. Figure 8A illustrates the underside of an individual that had been prised off its substratum, presumably during collection. The appearance of the cement accumulations around circular areas or little of no cement suggests that the substratum had been a poorly lithified sandstone and that the cement had pooled in the spaces between the grains. The extra-periostracal nature of this cement can be confirmed by the presence of debris, either shell fragments or mineral grains, trapped within the cement (Fig. 8C). It has proved difficult to establish the precise nature of the cement, despite intensive investigation. However, it does seem that it is predominantly organic rather than calcareous. This conclusion is based on two lines of evidence: (i) the bond is easily broken after immersion in bleach (Harper, 1991b), and (ii) during acid preparation, although the cement etches slightly back from the periostracum and non-calcareous inclusions (Fig 8B,C), it does so far less than either the shells of the myochamid itself or the host eucrasstellid, and shell material trapped within it. Furthermore, the cement lacks the orderly crystalline appearance of the calcareous cements of oysters (Harper 1992, 1997) having instead a sponge-like texture. In fact no crystalline material, other than trapped material, was observed. Nevertheless, spot elemental analysis of the cement layer has revealed a significant calcium peaks indicating that there is at least some calcium carbonate present. Further investigation of the cement is required, perhaps on fresher material, perhaps grown on selected substrata which favour the analysis (Harper 1992). Internal anatomy

Figure 8. Scanning electron micrographs of the cement layer of Myochama anomioides. A. Detail of the cementing surface of an individual which had been prised away from its substratum; scale bar 100 m. B. Etched section through the cemented right valve of an individual attached to the periostracum of an eucrassatellid shell (e); scale bar 10 m. C. Etched section through the right valve of an individual cemented to an eucrassatellid shell, note the presence of alien shell debris trapped within the cement; scale bar 100 m. C cement, P Periostracum of the right valve.

The basic features of the body of Myochama anomioides are shown in Figure 9, as seen from the right side and with the right mantle lobe removed. The plicate ctenidia are large and of the typical anomalodesmatan plan in comprising long inner demibranchs (ID) and reduced outer ones (OD) represented by the descending lamellae only. The left and right ctenidia are equal and attach to the visceral mass and mantle by ciliary junctions, again as in other anomalodesmatans. Ctenidial ciliation is thus of


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Figure 9. Myochama anomioides. The organs of the mantle cavity, as seen from the right side (For abbreviations see p. 414).

type E (Atkins, 1937). The labial palps (LP) are small, with no more than five or six sorting ridges. Valve inequality is not reflected in the organs of the mantle cavity. The visceral mass contains the intestine which is similar in length to that of Myadora striata and the style sac and mid gut are conjoined. The ovaries (O) are located dorsally in the visceral mass, the testes (T) ventrally. The sectioned specimen was mature with large telolecithal eggs (150 m in diameter), each of which was enclosed in a thick (25m) gelatinous coat as in Entodesma cuneata Gray (Campos & Ramorino, 1981) and Laternula elliptica (King & Broderip) (Ansell & Harvey, 1997) suggesting that larval development is brief and completed inside a protective demersal capsule. Sperm were contained within the supra-branchial chamber of the inner demibranchs. The digestive diverticula (DD) surround the stomach antero-dorsally, and the rectum (R) traverses the ventricle of the heart (H) postero-dorsally. The paired kidneys (K) lie beneath the pericardium (P). Valve inequality is thus not reflected in the visceral mass. This is best seen with respect to the nervous system. The pedal ganglia are symmetrical as are the statocysts (STAT) that are closely applied to them (Fig. 10). The statocysts are of Type B3 (Morton, 1985) in that each contains a number of inorganic, non-staining, irregular, statoconia (ST), one of which, the statolith (STA), is larger. They stimulate cilia (C) on the inner epithelium of the statocyst capsule. The posterior siphons (Fig. 9), inhalant (IS)

Figure 10. Myochama anomioides. A transverse section through the pedal ganglia and statocysts (For abbreviations see p. 414).

and exhalant (ES), are approximately equal in shape and length and do not appear to possess apical crowns of sensory papillae. They are separate at their tips and are formed by pallial fusions of type A (Yonge, 1957). There is a small pedal gape (PG) antero-ventrally. The foot is small, in common with that of many cementing bivalves, e.g. Cleidothaerus maorianus (Morton, 1974). Mid ventrally (MM), however, there is extensive mantle fusion, this involving the left and right inner folds and the inner surfaces of the middle folds, i.e. type B (Yonge, 1957) (Fig. 11). The margin of the right mantle lobe comprises a capacious haemocoel, inner and outer surfaces being cross-connected by muscle fibres (TF). The left lobe is more bulbous than the right and the haemocoel less strongly cross-connected. The pallial retractor muscle (PRM) in each lobe is attached deeply within the shell margin and comprises two components, the

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pseudofaeces, there are few glands and small pallial nerves (PN). Valve inequality as a result of the cemented habit in Myochama anomioides is, therefore, only reflected in the structure of the ventral mantle margin and the left and right periostraca that it secretes. As in Myadora striata (Morton, 1977), there are no arenophilic glands. DISCUSSION

Figure 11. Myochama anomioides. A transverse section through the fused mantle margin posterior to the pedal gape (For abbreviations see p. 414).

inner one of which passes towards the centre of the pallial union, the outer passing into the outer folds. The inner surface of the outer fold secretes the periostracum, as is normal for bivalves. The periostracum arises from each periostracal groove as a thin undifferentiated layer which progressively enlarges forming a thin ruffled outer, unstaining, layer (OP) and a thicker inner unstructured one (IP) which stains blue in both stains used, i.e. it is mucoid. At the shell margin, however, especially on the left, the outer periostracal layer quickly loses its ruffled appearance and, reflected over the shell forms a thick (12 m), yellow, sheet, the inner surface of which has a dimpled appearance. The inner periostracal layer, moreover, still staining blue, appears to have become delaminated into thin layers which have twisted over to lay parallel to the plane of the section (and thus each are of the thickness of the histological section) creating an overall appearance of being much thicker (30–50 m) than the outer. The outer layer, as noted earlier, dorsally forms the thick pad of ‘secondary (fused) ligament’. It also gives the unattached, left, valve its yellow colour. In other respects, the mantle margin is essentially similar to that described for Myadora striata by Morton (1977). The inner epithelium is ciliated for the collection and removal of

In the absence of any other recognised myochamid genera it seems reasonable to suggest that the cementing Myochama evolved from the more geographically widespread and geologically older Myadora (Upper Eocene— Recent) (Beu & Maxwell, 1990), some time before the Upper Oligocene. Both genera are highly inequivalve and, at first sight, appear similar. They are, however, mirror images of one another. Myadora has a flattened left valve whereas in Myochama it is the right which is flattened. Both animals adopt a life position with the flatter valve ‘morphologically’ lower; i.e. Myadora lies on its left valve within the sediment (Morton, 1977, Fig. 1) and Myochama cements by its right valve. Such morphological inversion occurs elsewhere among the bivalves, for example, it must be invoked in the early evolution of the predominantly dextrally pleurothetic Pteriomorphia in order to account for the oysters’ attachment by their left valve (Newell & Boyd, 1970). Presumably such inversion may be attained relatively easily by genetic mutation, and is known for other organisms, e.g. flounders (Hubbs & Hubbs, 1945). The lack of recognised myochamids which attach by the left valve suggests that inversion pre-dated the acquisition of the cemented habit. It is tempting to speculate that perhaps there are vital differences in the character of the myochamid left and right mantle lobes which prevent sinistrally pleurothetic forms from cementing but preadapt those resting on the right valve to do so. In most anatomical respects Myochama anomioides is simply a cemented Myadora, there being little, if any, significant difference between representatives of the two genera, at least in terms of their fundamental body plans. The anatomies of Myadora striata and Myochama anomioides are very similar and such differences as do occur, notably with regard to the presence of a well-developed foot and pedal retractor muscles in the former and the reduced foot and lack of associated muscles in the latter, relate to the adoption of the cemented habit.


There are also few differences between the left and right mantle lobes of the two species; although despite valve inequality, the mantle lobes of Myadora striata are equally well developed while in Myochama anomioides the left lobe is larger. In terms of shell construction, there are some notable differences between Myadora striata and Myochama anomioides. Whereas the periostraca of M. striata and those non-cementing parts of M. anomioides are similar, that of the latter during cementation is distinctly different. During cementation the sheet thins and gains a quilted appearance. This change in periostracal character during cementation may be analogous to the thinning of the periostracum in actively cementing Etheria elliptica Lamarck noted by Gregoire (1974). This thinning may be vitally important for the attachment process in these taxa which generally possess rather substantial periostraca, in that it is a critical requirement for the shell to be laid down in intimate association with the micro-topography of the substratum to allow adhesion to occur (Harper, 1992). The shell microstructure of Myochama anomioides also differs from that described for Myadora brevis, M. striata and M. tasmanica by Taylor et al. (1973) in the reduction of the outer prismatic shell layer into a series of protuberances. This study has shown that the right valve of Myochama anomioides is attached to its substratum by an extra-periostracal cement composed chiefly of organic material. The lack of arenophilic glands in both Myadora and Myochama allows us to reject the hypothesis that such glands may be responsible for cementation in this taxon. The organic-rich cement layer, is likely to be discharged from other glands within the mantle, although none of the individuals examined in this study showed any material adhering to the outside of the periostracal sheet as it emerges between the mantle folds, nor did the single specimen examined histologically reveal any glands which might be suitable candidates for such secretions. The reason for this failure to find the glands responsible for cement production in Myochama anomioides may be because the specimens examined were mature and had ceased actively to cement; indeed many had right valves which had lifted ventrally from the substratum. Both fossil and living members of Myochama have a preference for colonising living, shallowburrowing, bivalves, in particular large taxa, and we suggest that the myochamid derives some benefits from the association. Not only is

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it necessary for the siphons of M. anomioides to point towards the sand-water interface but there is potential benefit in the coincidence between the inhalant current directions of host and symbiont. There are also advantages associated with attaching to larger host taxa. Whereas Myadora is able to respond to exhumation by re-burrowing rapidly, Myochama may avoid this energetically expensive necessity by attaching to larger, more stable bivalves which are less likely to be dislodged. It is also possible that attachment to larger hosts may effectively increase the size of the myochamid which may then gain some protection from predators which manipulate their prey, e.g. asteroids and crustaceans, and thus attain a size refuge. The relationship between myochamids and infaunal bivalves is, however, not an obligate one. Rocks and empty shells may also serve as substrata. The relative size, however, of nepioconchs in these examples suggests that they are only selected when other, more suitable, substrata are unavailable and when the process of metamorphosis and cementation cannot be delayed any longer. Yonge & Morton (1980) suggested that in order for Myochama anomioides to capitalise on their specialist substratum requirements, the species probably employs direct development, involving incubation of the postlarvae. They supported this hypothesis with the observation that potential space is available for this in the bag-like inner demibranchs and the fact that small and large myochamids occur on the same host. The single specimen of M. anomioides sectioned in this study was sexually mature with large, telolecithal eggs surrounded by a thick coat of mucus. Similar eggs have been reported upon for numerous species of anomalodesmatans and it is suggested that their development is either direct or that the larval life is short (Allen, 1954; Campos & Ramorino, 1981). Ansell & Harvey (1997), however, show that development in Laternula elliptica inside its solidified mucus egg capsule is not rapid ( 22 days and in fact probably many times that (L.S. Peck, personal communication)) but this may be a result of its Antarctic distribution. Comparison of the size of the prodissoconch of Myochama anomioides measured in this study with the model produced by Ockelmann (1965) suggests that development of this taxon at least is likely to be direct. The large size of pre-cementation individuals of Myochama anomioides (height 1.2–3.9 mm) suggests that cementation occurs relatively late in ontogeny, probably after a period of weak

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byssal attachment as has been described for the majority of bivalve taxa (Yonge, 1962) although no evidence for this has been discovered in this study. In other cementing bivalves, e.g. species of Ostreidae, Dimyidae and Plicatulidae (Yonge, 1979), cementation follows rapidly after settlement from the plankton, although that in Hinnites ( Crassadoma) it occurs very late in ontogeny, perhaps after attainment of sexual maturity (Yonge, 1951). The evolution of the cemented habit in the Myochamidae may be regarded as part of the evolutionary trend within the Pandoroidea, perceived by Morton (1977), towards more sedentary life-styles. The evolution of cementation from an infaunal ancestor is effectively the transition between an infaunal and epifaunal life habit and represents a different way of achieving this from the better known endobyssate- epi-byssate route described for the mytiloids (Stanley, 1972). Cementation in the Cleidothaeridae, another exclusively Australasian pandoroid family, appears to have evolved at a similar time during the Miocene (Beu & Maxwell, 1990), although there is no obvious selection pressure that might account for this coincidence.

L LP LV ME MM O OD OMF OP P PA PEG PG PHT PL PN POL PR PRM PS R RV STA ST STAT T TF TT U

Lithodesma Labial palps Left valve Mantle epithelium Mantle margin Ovary Outer demibranch Outer mantle fold Outer layer of periostracum Pericardium Posterior adductor muscle (or scar) Pedal ganglia Pedal gape Posterior hinge tooth Pallial line Pallial nerve Posterior outer ligament layer Prodissoconch Pallial retractor muscles Pallial sinus Rectum Right valve Statolith Statoconia Statocyst Testis Transverse fibres Tongue of tissue Umbo

ACKNOWLEDGEMENTS

REFERENCES

We are grateful to the Royal Society of London for providing BM with funds to undertake this research and for EMH’s Royal Society University Research Fellowship. EMH initiated this work whilst on an Australian Museum Visiting Fellowship, for which she was grateful and also to Tom Darragh and Sue Boyd for allowing her to examine the collections of the National Museum of Victoria. This is Cambridge Earth Sciences Publication Number 5854.

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Key to abbreviations used in Figures AA AHT AOL C DD DMV ES FIMF ‘F’P F H ID IL IP IS K

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