Byssus-attachment by infaunal clams: Seagrass-nestling Venerupis in Esperance Bay, Western Australia (Bivalvia: Veneridae)

F.E. Wells, D.I. Walker and GA. Kendrick (eds) 2005. The Marine Flora and Fauna of Esperance, Western Australia. Western Australian Museum , Perth.

Byssus-attachment by infaunal clams: Seagrass-nestling Venerupis in Esperance Bay, Western Australia (Bivalvia: Veneridae) Rudiger Bieler 1, Paula M. Mikkelsen 2, Robert S. Prezant 3 1

2

Department of Zoology, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2496, U. S. A. Email: [email protected]

Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79'h Street, New York, New York 10024-5192, U.S. A. Email: [email protected] 3

Department of Biology and Molecular Biology, Montclair State University, Montclair, New Jersey 07043, U. S. A. Email: [email protected] Abstract - Venerupis galactites (Lamarck, 1818), an endemic Australian infauna! venerid clam, is morphologically/anatomically described based on specimens collected in shallow-water Posidonia australis seagrass beds in Esperance Bay, Western Australia. The species lives in high densities (l ,300/m 2) in 2-4 cm sediment depth, byssally attached to the seagrass rhizome mats. Notable features of its anatomy include elongated siphons that are united nearly to the tip, expansive plicated gills, and a prominent byssal groove on the posteroventral foot. The byssal gland in histological sections is irregularly ovoid and cupulate, with a narrow lumen; the microfibrillar ribbon-like byssus forms a single thick proximal stalk that divides distally into 2- 3 branches. Each branch can have numerous periodic, flat and parallel side-branches that extend from one side of the primary byssal thread and terminate in attachment plaques. The form of the byssus is reflected in the byssal duct, which has an infolded secretory epithelium that forms or molds the side branches. Byssal attachment by adult clams is discussed for the largely free-living and infauna! family Veneridae, a group in which neotenous retention of this postlarval feature was thought to be restricted to intertidal rock nestlers. Rather than representing a simple retention of neotenous features, the elaborate byssal apparatus of V galactites is clearly derived. The parallel side branches seen along a single side of the primary byssal threads could reflect an adaptive feature for secure adhesion in an infauna! life mode nestled along relatively narrow, cylindrical rhizomes. Key words: Veneroidea, Posidonia, anatomy, byssal gland, ecology, histology, neoteny

INTRODUCTION The bivalve byssal gland is thought to have evolved as a postlarval structure that provides anchorage until the young animal is securely anchored in the substratum (Yonge, 1962). The pediveliger byssal apparatus is widespread, if not universally present in the Bi val via (but often overlooked, see Carriker, 1990), and might or might not be retained into adult life. The western Atlantic hard-shelled clam Mercenaria mercenaria (Linnaeus, 1758) (Veneridae), for instance, forms a weak byssal attachment for some time after metamorphosis (Carriker, 1956). Later during ontogeny the byssus is no longer used in such free-burrowing species, when stabilization and deeper penetration into the substratum is accomplished by shell costae as well as increases in size and weight (Stanley, 1972). By contrast, neotenous retention of the byssus-producing

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organ (byssal gland) has provided a major avenue for those bivalve groups that developed epifaunal (e.g. , Mytilus) or only partially substratum-embedded (e.g., Pinna) modes oflife. The vast majority of the large "Venus clam" family Veneridae lives infaunally and does not retain the byssus into adulthood. The known exceptions among venerids are distributed over several of the 12 nominal subfamilies, an indication that neotenous retention has occurred repeatedly in this group. The best known examples include Nutricola tantilla (Gould, 1853) and its recently separated congener N. confusa S. Gray, 1982, both shallow-burrowing eastern Pacific species of Pitarinae in which adult shells measure only a few millimetres, i.e., in the size range of a byssate Mercenaria juvenile. Narchi (1970; describing Transenella [= Nutricola] tantilla) argued that the byssus anchoring the animal to sand grains would prevent dislocation of the small adult shell by water movements, and also might play a role in brood protection in this ctenidial-pouch brooding species. In a larger-shelled burrowing chionine venerid, Timoclea scabra (Hanley, 1845), the byssal gland remains functional in only some adults (Narchi, 1980, as Veremolpa scabra) and the ability to produce a single thread of byssus might have some residual anchoring function for these individuals. Some members of the subfamily Tapetinae have ventured into the rocky intertidal where they nestle, attached by stout adult byssi, in crevices and/or among other bivalves and polychaetes. These byssate nestlers include the carpet shell Venerupis corrugata (Gmelin, 1791) [as described by Quayle, 1949, from Scotland; as V. pullastra (Montagu, 1803)] and lrus macrophyllus (Deshayes, 1853) [as described by Morton, 1985, from Hong Kong; as I. irus (Linnaeus, 1758)]. The present paper describes an infauna!, burrowing tapetine venerid that nevertheless retains functional byssal attachment into adulthood. Venerupis galactites (Lamarck, 1818), known in the Australian literature as "Milk Stone", is widely distributed along the Australian coast and was originally described from the south shore of Western Australia. From specimens observed in shallow waters off Esperance, Western Australia (Figures 1-3), it is demonstrated to be a burrower that attaches to sediment-embedded rhizome mats of the seagrass Posidonia australis Hook. A study of this species also provides an opportunity to give detailed anatomical data for a member of the still ill-defined nominal genus Venerupis Lamarck, 1818.

MATERIALS AND METHODS Living specimens were randomly collected by RB, John Taylor and Emily Glover with shovel and sieve from a Posidonia meadow in front of the sandy shore of the Esperance Bay Yacht Club, Western Australia (33 °51.90'S, 121 °53.65'E), in 1-1.5 m water depth, 6-16 February 2003 (stations FMNH/RB-1823, 1827, 1839, 1848), initially in part as a by-product of searches for other bivalve groups. Small samples of P australis and attached clams were transported to the field lab for further observation and dissection. 120 individuals were measured for maximum shell length (using calipers) and observations were made on their tentacle pigmentation and coloration of their umbonal shell regions. In addition, a quantitative sample was taken by corer and shovel, removing Posidonia seagrass and surrounding sediment equivalent to 20 x 20 cm surface area to a depth of approximately 10 cm. Photographs were taken of attached clams and all living individuals were counted and measured (length, height and inflation). Additional collections of empty shells were made, by shovel and sieve and hand-collecting during scuba dives, at various seagrass localities in the greater Esperance region and in the offshore Recherche Archipelago. For anatomical observations, living specimens were relaxed by chilling in a household refrigerator assisted by the addition of magnesium sulfate crystals (Epsom salts) to their

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Figures 1-3

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Venerupis galactites, living animals as collected in Esperance Bay. 1, in situ on rhizome mat of Posidonia australis, after removal of sediment; 2, close-up of left posterior of specimen with partly extended siphons; note arborescent tentacles on (lowermost) incurrent siphon; 3, left lateral view of individual attached by byssus (arrow). Length of shell in Figures 2- 3 = 32 mm.

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seawater supply, or in an isotonic aqueous magnesium chloride solution. Anatomical details were observed under a dissecting microscope; preserved tissues were dyed for better contrast with neutral red or methylene blue. Voucher specimens were fixed in 5% formalin , later transferred to 70% ethanol, and are deposited in the Field Museum of Natural History, Chicago (FMNH 302016-302025, 302054-302055), the American Museum of Natural History, New York (AMNH 311150), and the Western Australian Museum (WAM S 13497). Soft parts (foot, byssus) were critical-point-dried for SEM. SEM photomicrographs were taken of gold-coated specimens on an Amray 1810 scanning electron microscope at FMNH. To enhance the appearance of muscle scars and pallial line, the shell used for the inside view (Fig. 6) was briefly immersed in diluted household bleach (aqueous sodium hypochlorite) before mounting for SEM. For histochemical studies of the byssal gland, excised feet were embedded in paraffin, sectioned at 6-7 µm and stained with alcian-blue/periodic acid/Schiff (PAS), alcian-blue at pH 2.8 with nuclear fast red, or toluidine blue (sodium borate buffered). RESULTS Veneroidea: Veneridae Rafinesque, 1815 (as Veneridia) Tapetinae J.E. Gray, 1851 (as Tapesina)

Venerupis Lamarck, 1818

Type species by subsequent designation (Children, 1823a: 303): Venus perforans Montagu, 1803 [= Venus saxatilis Fleuriau de Bellevue, 1802; see Discussion] Venus galactites Lamarck, 1818: 599, no. 52. Venus galactites , - Hanley, 1842 in 1842- 1856: 123. - Hanley, 1856 in 1842- 1856: pl. 15, fig. 51. - Pfeiffer, 1870 in 1841- 1872: 224-225, pl. 38, figs. 6, 7. Venerupis galactites, - J.E. Gray, I 827: [240]. - Hedley, 1918: M25 . - May, 1921 : 24. - Lamy, 1922: 82. - May, 1923: 27, pl. 11, fig. 1. - Cotton and Godfrey, 1938: 248, fig. 275. - Cotton and Godfrey, 1940: 15. - Cotton, 1946: pl. 2, fig. 32. - Allan, 1950: 335. - Macpherson and Chapple, 1951: 152. - Allan, 1959: 335. - Cotton, 1961: 263 , fig. 183. - Fischer-Piette and Metivier, 1971: 10-11. - Wells and Bryce, 1986: 176, pl. 68, fig. 640. - Ludbrook and GowlettHolmes, 1989: 674-676, fig. II.50e, f. - Wells and Bryce, 1988: 176, pl. 68, fig. 640. - Jansen, 2000: 100, fig. 403. Tapes galactites, - G. B. Sowerby II, 1853 in 1847- 1887: 695-696, pl. 151 , fig . 132. Deshayes, I 853: 183, no. 66. - Reeve, 1864: pl. 12, fig. 65. - Romer, I 871 in 1870-1872: 9394, no. 72, pl. 32, figs. 3, 3a, 3b. - Tate, 1887: 91. - Tate and May, I 901: 429. - Pritchard and Gatliff, 1903 : 134. - Lamy 1923: 280. - Iredale and McMichael, 1962: 23. Tapes (Cuneus) galactites, - H. Adams and A. Adams, 1857 in 1854- 1858: 436. - Angas, 1865: 650,no.48. - Angas, 1877: 192,no.17. Venus (Tapes) galactites, - Romer, 1864: 80. Venerupis (Pullastra) galactites, - Jukes-Brown, I 914: 93. Paphia galactites, - Hedley, 1916: 16. Pullastra galactites, - Lamy and Fischer-Piette, 1939: 465. - MacPherson and Gabriel, 1962: 356, fig . 413 .

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Pullustra [sic] galactites, - May and Macpherson, 1958: 15, pl. 11 , fig.1. Irus galactites, - Wells and Bryce, 1984: 80. Venerupis (Venerupis) galactites, - Lamprell and Whitehead, 1992: pl. 77, fig. 613. Type locality

Originally given by Lamarck (1818) as "Jes mers de la Nouvelle Hollande, ou port du Roi George" [= King George Sound, outer harbour of Albany, south coast of Western Australia; about 35°6'S, 1l8°E] . Type material (Figure 4):

Syntypes in the Lamarck collection at Museum National d'Histoire Naturelle (MNHN), Paris, as described by Lamy and Fischer-Piette (1939: 465), consisting of two individuals: a single

Figure 4

Syntypes of Venus galactites Lamarck, 18 18 (MNHN Lamarck collection).

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right valve (60 x 35 mm) of one, and both valves of another (42 x 25 mm). The material was collected by Charles-Alexandre Lesueur and Franc;ois Peron on their Australian expedition in 1803. Shell Shell (Figures 5, 6) moderately sized (mostly < 40 mm, but known to reach 60 mm), relatively thin but solid, equivalve, elongated oval, with nearly straight dorsal margin and obliquely truncated posterior margin; inequilateral with low, rounded um bones ca. 1/5 of the shell length from the anterior end. Longer than high (length to height ratio 1.62, n = 40), and moderately inflated (inflation to height ratio 0.36, n = 40); these proportions apparently varying among populations, evidenced by museum specimens with L:H 1.75 and I:H 0.74 (AMNH 31568, "Australia'', ex Haines Collection acc. 1895, n = 5), and by Romer 's (1871 in 1870-1872: pl. 32, fig. 3, lb) figures with L:H 1.63 and I:H 0.63. External sculpture consisting of coarse commarginal growth striae, becoming somewhat erect posteriorly (Figure 7) and especially anteriorly; commarginals crossed by low, flattened radial ribs separated by shallow grooves, higher anteriorly where they cause undulation of the commarginal ridges. Lunule elongate, with barely incised margin, asymmetric, right half slightly larger than left, with fine commarginal lamellae, without radial elements. Escutcheon not delimited by marginal groove, distinctly larger in left valve, right edge overlapping left in the posteriormost third, both halves finely obliquely grooved. Colour uniformly milk-white, interiorly and exteriorly, occasionally with some yellow staining at posterodorsal angle; periostracum non-persistent. Internal margin smooth. Both adductor muscle scars teardrop-shaped; posterior adductor muscle scar slightly broader; dorsalmost portion of posterior scar formed by pedal retractor muscle scar, weakly demarcated. Anterior pedal retractor muscle scar on ventral side of hinge plate, dorsomedial to anterior adductor muscle scar (and connected to it by a narrow band), just below anterior cardinal tooth. Pallial line entire; pallial sinus wide, broadly pointed, extending anteriorly to approximately anterior-posterior midpoint of shell. Accessory pallial muscle scars just inside pallial line, moreor-less regularly spaced. Hinge teeth of each valve (Figures 9, 10) comprising three subequal cardinal teeth; anterior (2a) and middle (2b) of left valve, and middle (1) and posterior (3b) of right valve, are bifid; lateral teeth absent. Prodissoconch (Figure 8) smooth, distinctly marked by PI (embryonic; 180- 210 µm, n = 5) and PII (390-440 µm length, n = 5) growth stoppages. Umbones often tipped with greyish purple markings that occasionally extend as a narrow radial flame onto the juvenile shell. Anatomy Entire softbody (Figures 11 , I 2) translucent white in living specimens, except for flocculentwhite gonad and brown digestive gland showing through visceral mass; occasional specimens with faint orange-brown staining along mantle edge and around byssal opening, as well as darker tips of siphons (see below). Pedal gape extending ventrally from base of incurrent siphon to anterior adductor muscle; margin finely papillate. Siphons extensible to 1.5 times shell length in living animals, fused along most of their length, separate at terminal 1/5; each end with black surface pigment (Figure 2) and orange-brown lining in widely varying densities, and capable of closing sphincter-like. Each siphon internally with opaque white dots (in preserved specimens) extending from terminus to halfway mark of total length. Each siphon with basal siphonal membrane (proximal valve) consisting of a thin tissue flap narrowing the lumen. Incurrent

BYSSAL-ATTACHING VENERUPIS

Figures 5-10

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Venerupis galactites shell, Esperance Bay (SEM, FMNH 302054). 5, exterior of right valve (22 mm length); 6, interior of right valve (18 mm length); 7, detail of posterior shell surface of specimen in Figure 5; 8, Prodissoconch of shell in Figure 10; 9, hinge detail of left valve; 10, hinge detail of right valve. Abbreviations: I, right middle cardinal tooth ; 2a, left anterior cardinal tooth; 2b, left middle cardinal tooth ; 3a, right anterior cardinal tooth ; 3b, right posterior cardinal tooth; 4b, left posterior cardinal tooth ; lg, ligament, PI, prodissoconch I; PII, prodissoconch II. Scale line = I mm in Figures 7, 9, 10; I 00 µm in Figure 8.

(ventral) siphon slightly larger in diameter and length than excurrent (dorsal) siphon, with finely branched (arborescent) terminal tentacles (Figure 2); excurrent siphon tapering to narrower terminal diameter than wider, slightly flaring incurrent siphon, with simple elongate terminal tentacles and incomplete valvular membrane just interior to tentacled margin. Demibranchs plicated (outer demibranch [OD] with ca. 15- 21 plicae, inner demibranch [ID] with ca. 19- 25 plicae; n = 8), with axes nearly vertical and filaments oriented nearly anteroposteriorly; ID approximately twice as large as OD. Food groove present at distal edge of ID only; cilial

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11

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Figures 11-12

Venerupis galactites anatomy, composite sketches from living and preserved specimens (about 32 mm shell lengths). 11, Animal as seen from the right side with right shell and mantle removed; bold hatch marks at dorsal anterior and posterior indicate points of mantle fusion. 12, Ventral aspect of gaping animal, with siphons fully extended. Abbreviations: aam, anterior adductor muscle; aprm , anterior pedal retractor muscle ; ba, bulbus arteriosus; by, byssus; es, excurrent siphon; ft, foot; h, heart; id, inner demibranch ; in, intestine; is, incurrent siphon; lp, labial palps; od, outer demibranch ; pam, posterior adductor muscle; pg, pedal groove; pprm , posterior pedal retractor muscle; sm , siphonal muscle; st, stomach.

currents of gills, palps and mantle surface not determined. Triangular palps elongate, with narrow lamellae on inner surface (31- 37 lamellae, n = 8); margins smooth at ventral and dorsal side; outer surface smooth. Oesophagus relatively short, leading into anterior part of small stomach; stomach embedded in digestive diverticula, posterior to labial palps. Style sac combined with midgut, together exiting posteroventrally from posterior end of stomach, then turning anteriorly and coiling on ventral side of stomach, turning again posteriorly ventral to style sac, then ascending (as hindgut, penetrating pericardium, ventricle and bulbus arteriosus) to continue dorsally and posteriorly across surface of posterior adductor muscle to end as anus. Stomach filled with fine

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14

Figures 13-14

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Venerupis galactites, details of foot and byssus. 13, Detail of byssus (artificially straightened from preserved specimen, exact orientation of attachment plaques not ascertained). 14, Light photomicrograph of emerging byssus (preserved specimen). Abbreviations: bap, byssal attachment plaque; ft, foot; pbt, primary byssal thread; sbt, secondary byssal thread. Scale lines = 2 mm in Figure 13; 1 mm in Figure 14.

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particles, diatom frustrules, and organic debris (from histological sections). Kidney surrounding pericardium and heart. Three pairs of ganglia, with cerebral ganglia between anterior pedal retractor and adductor muscles, joined by supraoesophageal commissure. Gonad surrounding stomach and intestine within visceral mass; testes of male extensive, penetrating deep into foot; reproductive system not otherwise investigated. Foot large, anvil-like, pointed anteriorly and posteriorly; byssal opening prominent, extending anteriorly as pedal groove leading to a prominent deep oval byssal pore, and continuing

Figures 15-16

Venerupis galactites, critical-point dried byssus (SEM). 15, Oblique view of underside of foot (posterior to the left), showing emerging byssus and attachment plaques with remnants of seagrass tissue. 16, Secondary byssal thread terminating in attachment plaque, with remnants of seagrass tissue. Abbreviations: bap, byssal attachment plaque; bp, byssal pore; er, crest; ft, foot; pg, pedal groove; sbt, secondary byssal thread; sgt, seagrass tissue; str, striae. Scale lines = 2 mm in Figure 15; 100 µmin Figure 16.

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posteriorly as a narrow smooth-bordered groove (Figure I 5, I 7); muscular with outer layer of circular muscle fibres overlaying blocks of longitudinal fibres and interspersed obliques. Foot epithelium densely ciliated; ventral epithelium with dense array of mucus-secreting pedal glands staining blue with alcian blue and beta metachromasia reactive with toluidine blue (Figure 20) (together suggesting acidic mucopolysaccharide secretion); with vacuolate array of weakly PASpositive secretory cells and an array of small sinuses deeper within pedal tissue. Large pedal ganglia abutting base of lamellate byssal gland. Byssal gland showing as opaque white glandular area (in living specimens) near the centre of the sole; irregularly ovoid to cupulate in histological longitudinal sections (Figures 17, 20), with relatively narrow lumen, communicating with exterior via elongated broad byssal canal. Byssus gland composed of surrounded amorphous secretory gland and cupulate or lamellate region composed of secretory cuboidal cells making up a series of short thin secretory tubules. Lamellate portion ofbyssus feeding into small ducts that release byssal precursor secretions into small-volume sinus-like area. Sinus-like area narrowing into byssal canal proper where byssal thread is molded. Ventral epithelium of canal and groove composed of tall columnar cells staining light pink with PAS, beta metachromatically with toluidine blue and containing granules staining positively with alcian blue at pH 2.8. These cells with large ovoid nuclei and short border appearing lined by microvilli ("brush" border under light microscopy). Invaginations of ventral canal epithelium creating series of short finger-like depressions. Within byssal groove and canal, precursors of secondary byssal branches aligning perfectly with grooves formed by invaginations in ventral canal epithelium (suggesting that they are either secreted or molded within the duct proper; Figures 18, 19). Dorsal and dorsolateral byssal duct epithelium relatively smooth but also with periodic invaginations. No byssal branches found associated with the latter. Columnar cells of dorsal epithelium of canal shorter and with smaller, less distinct ovoid nuclei. Bright blue (alcian blue positive) layer covering dorsal lumen epithelium representing a secreted acid mucopolysaccharide. Byssus consisting of single thick translucent stalk with microfibral texture. One to three ribbon-like primary byssal threads (approx. 200-300 µm wide) emerging from byssal pore (Figures 13, 14, 17). When detached from substratum, threads forming a tangled mass (Figure 15). Individually, however, primary threads possess a series of flat secondary branches that can be closely packed (as many as 4-5 per mm primary byssal thread length) along one side of primary ribbon (Figure 13). Secondary branches averaging 150- 200 µmin width, each ending in adhesive pad-like plaque. Distal portion of secondary branch of byssus crests where feeding into plaque. Microfibrillar composition of byssus (proximal, distal and plaque) apparent in scanning electron micrographs (Figure 16; arrow).

Distribution and habitat

Widely distributed along the Australian shoreline, spanning New South Wales, Victoria, Tasmania, South Australia, and Western Australia (to Perth, teste Wells and Bryce, I 988). As already stated by Fischer-Piette and Metivier (1971), references to its occurrence in New Zealand (e.g., Reeve, 1864; Romer, 1871in1870-1872) appear to be in error. Angas (1865: 650) gave its "station" in South Australia as "in deep water." Ludbrook and Gowlett-Holmes (1989: 676) described its habitat in South Australia as "gravelly sand to mud in the littoral zone, often in Posidonia root mat to I 5 m depth." Cotton (196 I: pl. 2) described it as "between tides on sand

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Venerupis galactites, histogram of maximum shell lengths of live-collected specimens at study site in Esperance Bay (3-mm buckets).

flats." Specimens in this study were found in 1- 1.5 m water depth in a Posidonia meadow in front of a sandy shore, with individuals positioned 2-4 cm deep in the sediment, 3- 6 individuals per seagrass clump (Figure 1), with smaller clams nestling in branching parts. Local abundance and density can be very high: based on a single quantitative corer sample in the studied Posidonia meadow, the population density was calculated as 1,325 individuals per m 2•

Size range The live-collected animals (n = 173) at the study site ranged in length from 2.5-36.5 mm. Because of the coarse collecting technique (some small specimens were indubitably lost in the ..... Figures 17-20

Venerupis galactites, histological longitudinal foot sections. 17, Section of excised foot of adult 32-mm specimen (7 µm section, PAS/alcian blue), showing massi ve byssal gland, PAS-positive cells lining byssal canal and alcian blue-positive cells bordering pedal epithelium. 18-20, Section of foot tissue of 27-mm specimen. 18, Ventral byssal canal, showing infolded ventral epithelium corresponding to secondary byssal branches (PAS/alcian blue stain). 19, Detail of ventral byssal canal showing close relationship between byssal branches (arrow) and tissue invaginations (PAS/ alcian blue stain). 20, Lamellate byssal gland in longitudinal section (6 µm) , showing small ducts (circular in cross section) feeding into byssal canal. Beta metachromasia (toluidine blue stain) identifies a large, amorphous byssal gland proper surrounding most of the distal and lateral reaches of the lamellate gland. Abbreviations: be, byssal canal; bg, byssal gland; bo, opening of byssal gland; by, byssus; in, intestine, lbg, lamellate byssal gland; pg, pedal groove; sbt, secondary byssal thread; ve, ventral epithelium. Scale bars = 2 mm in Figure 17; 25 µm in Figure 18; 25 µm in Figure 19; 120 µmin Figure 20.

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silt and wave action), absolute values on the size-frequency diagram (Figure 21) should not be over-interpreted. Empty shells collected in other Esperance Bay seagrass areas in the vicinity ranged in size to 41 mm, indicating that the animals of the study population had not yet reached maximum shell size. The largest shell encountered, at 45.4 mm, was collected among Posidonia australis in Lucky Bay, Cape la Grand, southeast of Esperance (FMNH 302055, RB-1845). The species can reach even larger shell size, as seen in the MNHN type specimen at 60 mm (originally cited as 62 mm; Lamarck, 1818).

DISCUSSION Taxonomic placement and the genus Venerupis As can be seen in the synonymy listing, the species-level identity of this Australian endemic has not been debated, but its generic allocation has been in flux . Much of tapetine genus-level taxonomy has been based on different degrees of and combinations of radial and concentric sculpture, and involves various taxa such as Tapes Megerle von Miihlfeldt, 1811 (with concentric lines and ridges), I rus Schmidt, 1818 (with thin raised concentric lamellae ), Venerupis Lamarck, 1818 (with irregular raised concentric lamellae in later growth), and Ruditapes Chiamenti, 1900 (with decussate sculpture formed by concentric lines and radial striae). Hinge teeth seem to define two groups among these four genera: Venerupis and Irus (with narrow left middle cardinal tooth (2b), and posterior cardinal teeth (3b, 4b) perpendicular to hinge plate edge), and Tapes and Ruditapes (with wide left middle cardinal tooth (2b), and posterior cardinal teeth (3b, 4b) inclined relative to hinge plate edge) (Fischer-Piette and Metivier, 1971 ). The distinctions among these nominal genera are ill defined and most likely do not reflect natural groupings. Sufficient comparative anatomical and molecular data to further address this issue are not yet available. Most recent authors place this species in the tapetine genus Venerupis, introduced by Lamarck (1818) in the same work in which he described V. galactites - which he however placed in Venus. V. galactites has irregular raised concentric lamellae in later growth, and we therefore adopt this placement. Lamarck (1818: 506-508) introduced the genus Venerupis for a group of seven nominal species. These included two previously described taxa, Venus perforans Montagu, 1803 , from the United Kingdom , and Mediterranean Donax irus Linnaeus, 1758 (which later became the type of Irus) . The others were newly described, with Venerupis nucleus from the French Atlantic coast, and the remaining (V. exotica, V distans , V crenata, and V. carditoides) stemming from Frarn;ois Peron 's collections in Australia and the South Seas. Children (l 823a: 303) selected a type species by subsequent designation: Venus perforans Montagu, 1803, a nominal species subsequently considered a synonym of Venerupis saxatilis (Fleuriau de Bellevue, 1802) (e.g., Lamy, 1923, Barrett and Yonge, 1958) from the British Isles. V saxatilis is a relatively small-shelled (usually 20- 30 mm) morph that lives intertidally, attached by its byssus, in rock crevices and in holes vacated by rock-borers; its shell has concentric ridges that are raised and folded posteriorly, and often is distorted due to its habitat (e.g. , Beedham, 1972; Tebble, 1976). While these and other authors maintained its status as a valid species, V saxatilis was stated by some to be an ecophenotypic morph and synonym of the common and widespread European/Mediterranean species traditionally called Venerupis pullastra (Montagu, 1803) (e.g., Lamy, 1923; Panetta and Dell' Angelo 1977; Smith and Heppell, 1991: 88, "examination of growth series in situ has shown that the distortion

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characteristic of V saxatilis is merely a response to inadequate growth space"). However, the synonymy of this species remains confused. It involves three names that were simultaneously introduced by Gmelin (1791), as Venus corrugata, V geographica, and V senegalensis . Depending on which of these three were considered synonymous, and on what name was chosen as the "senior" synonym, subsequent authors thus called this species Venerupis corrugata (e.g., Lamy, 1923; Fischer-Piette and Metivier, 1971), Venerupis geographica (e.g., Panetta and Dell' Angelo, 1977), or Venerupis senegalensis (e.g., Bowden and Heppell, 1968; Smith and Heppell, 1991). Others (e.g., Nordsieck, 1969; Hoisreter, 1986) maintained the usage of Montagu's younger name, Venerupis pullastra. Bowden and Heppell (1968 : 261) credited Fischer-Piette et al. (1942) with first advisor action of selecting V senegalensis (based on the then-valid ICZN 1961 Article 24(a)), but overlooked the earlier work by Lamy (1923) who chose V corrugata as the senior synonym. Molecular data are needed to further resolve this variable species/complex, which ranges from Scandinavia to the Mediterranean and South Africa.

Byssal attachment Adult byssal attachment has been previously reported for members of the venerid subfamily Tapetinae. However, a well-developed adult-shell byssus heretofore was thought primarily restricted to species nestling in the rocky intertidal. In describing the functional anatomy of British veneroideans, Ansell (1961: 502) stated that the byssal gland of venerids is functional at settlement, but "only in Venerupis does it remain functional in the adult." Venerupis s. I. indeed has a relatively large number of famously byssiferous species. The byssus of V corrugata is large [see M. E. S. Gray, 1857: pl. 315 , fig. 2a, as Pullastra geographica ; Quayle, 1949: 31, as V pullastra]; this species has been reported to attach to rocks "buried an inch or two below the surface" (Quayle, 1949: 31), a situation very similar to the attachment of V galactites to Posidonia rhizomes. Also byssiferous are V decussata (Linnaeus, 1758) (often placed in Ruditapes; M. E. S. Gray, 1857; Pelseneer, 1911), V saxatilis (Tebble, 1976: 123), and "V quadrasi" (of unrecognized authorship; Pelseneer, 1911 ), as are the apparently closely related tapetines Irus irus (fide M. E. Gray, 1857) and I. macrophyllus (fide Pelseneer, 1911; Morton, 1985). The byssus of V corrugata was described as "single proximally ... [then] distally, where it is attached to the holdfast, it is divided into several strands" (Quayle, 1949: 31 , as V pullastra), radiating from the base of the initial stalk (M. E. S. Gray, 1857: fig. 315, fig. 2a). In all other cases the byssus has been illustrated as a thick clump of simple unbranched strands (V corrugata by M. E. S. Gray, 1857: pl. 313, fig. 7, as Venus pullastra; V "quadrasi" by Pelseneer, 1911: pl. 19, fig. 1; I. macrophyllus by Morton, 1985: fig. 2, as l. irus). However, none has been studied in detail, and it remains unknown whether the byssus in any other venerid shows a branching pattern like that found in V galactites. Rather than presenting a simple retention of neotenous byssus threads, the elaborate byssal apparatus of V galactites is a derived structure that upon wider investigation might prove a synapomorphy within or above the level of family Veneridae. Byssal production in adult venerids is now recognized in three other subfamilies, including Pitarinae [Lioconcha castrensis (Linnaeus, 1758), M. E. S. Gray, 1857; and Nutricola spp., mentioned earlier, see also Quayle, 1952], Gemminae [Gemma gemma (Totten, 1834), Sellmer, 1967; Narchi, 1971], and Chioninae [Timoclea scabra, mentioned earlier; and Chamelea striatula (da Costa, 1778), Ansell, 1962]. Byssus threads in these species have been described

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(if at all) as thin, single, and/or short (Narchi, 1971 , 1980), thus apparently less robust than in the tapetines. Sellmer (1967) never observed byssal threads in G gemma and supposed that the byssal gland added secretion to that of the pedal mucus glands to produce an adhesive substance allowing the animal to actively crawl up vertical surfaces. A byssal groove and rudimentary byssal apparatus have been noted in Circe sulcata Gray, 1838 (Pelseneer, 1911), but without proof of byssal production. The presence of a pedal groove has been observed in several other venerids [e.g., Circe corrugata (Dillwyn, 1817), Periglypta listeri (Gray, 1838), Venerupis bruguieri (Hanley, 1845); Pelseneer, 1911; Bieler et al. , 2004; unpubl. data], although byssal production has not been verified in adults of these species. The byssal gland of Venerupis galactites in histological section is irregularly oval and cupulate, with a narrow groove (Figure 17). That of the pediveliger of Chamelea striatula has a similar shape (Ansell, 1962: 423, figs . 4B, 8) as does Gemma gemma (see Sellmer, 1967: fig. 6), although lumina have not been described. A distinct lumen, T-shaped in cross section and narrow in longitudinal section, thus probably very similar to that in V galactites, was depicted for the byssal gland of V decussata by Carriere (1879: pl. 5, figs . lOA- B) and is commonly found in other heterobranchs [Arctica islandica (Linnaeus, 1767); see Carriere, 1879: pl. 6, figs . 12A- B]. There are variations in byssal types in bivalves that can reflect habitat and behaviour. Davenport and Wilson (1995) briefly described variation in relative byssal length and strength in four small brooding bivalves as they related to mobility, gregariousness and habitat. These authors were able to correlate the long elastic byssus of the cyamiid clam Gaimardia trapesina trapesina (Lamarck, 1819) with its byssally tethered home on the alga Macrocystis pyrifera (Linnaeus). The limopsid Lissarca miliaris (Philippi, 1845) lives attached to the complex red alga Schizoseris condensate (Reinsch) or on hard rock surfaces in surge channels. Its shorter but highly elastic byssus, radiating in several directions, also lends good stability. The galeommatoidean Lasaea rubra (Montagu, 1803), on the other hand, has very short and relatively weak byssi (only 12 µm in diameter) but this very small and mobile bivalve lives deep within the holdfast mat oflridescent Seaweed, Iridea cordata (Turner). Venerupis galactites has developed a secure byssus with tens of attachment plaques that align along the buried holdfasts of Posidonia australis. The non-radiating plaques follow in line and offer a secure attachment along a relatively narrow and non-shifting substratum. The alignment probably also offers resistance to weaknesses caused by the loss of individual plaques during any sediment shifting. The bases of the secondary byssal branches in Venerupis galactites form flat triangular attachment plaques. These plaques are similar to those of mytilids, spreading around a central elongated plate composing a central spongy matrix (Bell and Gosline, 1996). The widely splayed byssi ofmytilid mussels offer a clear adaptation to a mussel with full exposure to varied hydrodynamic conditions. Venerupis galactites on the buried rhizomes of Posidonia would not be so exposed. It is possible that the alignment of these secondary byssal branches along one margin of a primary ribbon-like byssal thread creates a strong rhizome-to-byssus connection. The finger-like projections of the secondary branches each ending in an adhesive plaque would offer a strong alignment along the narrow cylindrical rhizome. Attachment to the rhizome of buried seagrasses can only occur through a nonpolymerized region with a different composition. As noted, the plaque of Venerupis appears as a smooth pad-like area. In mytilids, the plaque has superficial fibres composed of a collagen-like matrix creating a spongy area (Benedict and Waite, 1986). The radiating byssal threads found in Mytilus edulis help secure the mussel within the unpredictable flow of water in rocky intertidal habitats (Bell and Gosline, 1996; Dolmer and

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Svane, 1994). Having attachment threads surrounding the mussel offers strong, multidirectional attachment in water flows that can enter and leave in almost any direction. In addition, the probing foot of M. edulis often ending in the addition of a byssal plaque gives the mussel an opportunity to sample a larger area of substratum and thus increases the chances of a secure attachment (Bell and Gosline, 1996). In most byssal glands an infolded glandular tissue offers an expanded secretory surface for production of byssal materials. It is not surprising then that the lamellate byssal gland found in Venerupis is at least superficially not unique. Gruffydd (1978) described a highly folded byssal gland in a cup-like structure for the scallop Chlamys islandica. Similarly, Prezant (1984) described a comparable structure for A nomia simplex d'Orbigny, 1842. In each case the lamellate byssal gland produced a ribbon-like byssus, which in A. simplex began as a thin mucoprotein template prior to calcification. In A. simplex, the form of the byssal gland is reflective of the calcified and lamellate byssus produced. It is uncertain (though unlikely) ifthe lamellate form of the byssal gland of V. galactites is involved in the production of the secondary, parallel branches of their ribbon-like byssus or whether these branches are formed in the grooves within the ventral byssal canal. In Venerupis the lamellate gland is surrounded by a broad, irregular mass of secretory cells that appear to feed into the lamellate and cupulate portion. The tubules of the lamellae can allow for increased secretory surface area or perhaps organization of the microfibres as they are released into the sinus-like chamber just outside the gland proper. At this stage the secretion must, however, still be fluid enough to be molded within the byssal canal and groove and as secondary branches are either added or molded from the non-polymerized byssal fluid. The byssal canal allows the addition of the secondary branches along one side of this highly aligned thread. The groove is the site of final molding and polymerization as the thread hardens into final form. Waite (1992) likened this process to polymer injection-molding. The byssus proper, throughout its length, appears in histological sections and light and scanning electron microscopic images to be composed of microfibrils. This confirms past observations that the byssus can be composed of micro filaments or fibres with a high collagen content (Bairati and Zuccarello, 1976; Benedict and Waite, 1986). In histological sections these microfibres can be discerned in the atrium just outside the byssal gland. Once they reach the byssal duct they have gained greater orientation running mostly in-line with the direction of thread growth. The ventral pedal epithelium is highly glandular, producing mucins in the form of acid mucopolysaccharides. These secretions could have a surface preparatory function prior to byssal attachment or might merely be lubricatory during pedal movement. The byssal gland proper also has a high component of acid mucopolysaccharide. It is here assumed that the observed byssal attachment to Posidonia (the only "hard" and ubiquitously available substratum in this shallow-water surf-zone environment) affords Venerupis galactites an anchor that helps prevent accidental dislocation from its shallow sediment burrow by wave action. This protection from dislocation is the same main advantage the byssus provides its relatives in the rocky-shore intertidal. However, there might be additional advantages in the case of V. galactites, such as providing a ready pathway for vertical movement to respond to silt load, oxygen levels, and availability of food particles. Stenton-Dozey and Brown (1994) have discussed the changes in the energy balance of South African V. corrugatus in response to tidal-influenced availability of natural suspended particles, and found an increase in filtering rate correlated with cyclic patterns of food supply. A closer look at the feeding behaviour and associated energy balance of V. galactities in its rhizome-associated habitat

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would be of great interest. Other ecological advantages for V galactites could be oxygenation from the plant itself because sediment around the seagrass rhizomes will be better oxygenated, as well as focused larval settlement. Barnes and Hickman (1999) discussed the ecology of a small lucinoid clam, Wallucina assimilis (Angas, 1868), that lives in similarly dense (1050/m2 ) populations in seagrass sediments at Rottnest Island, Western Australia. There are substantive differences between the species (W assimilis is smaller-shelled [usually < 10 mm], not byssally attached, and most notably carries bacterial symbionts providing chemautotrophy). Nevertheless, the causal relationship between these bivalves and their seagrass sediments seem similarly complex, involving physical, chemical, and biological factors.

ACKNOWLEDGEMENTS Thanks are due to Fred Wells, Di Walker, and Gary Kendrick for organizing the 12'h International Marine Biological Workshop in Esperance, and to the fellow participants for great company, interesting discussions, and various assistance. John Taylor and Emily Glover not only first pointed out the Venerupis population to RB but also supplied shovel, sieve, and muscle power for its exploration. Anne Brearley kindly shared her microscope, corer, and knowledge of the Australian seagrasses. Fred Wells and Alan Longbottom served as dive partners and shared their insight into the local molluscan fauna. Fred Wells, Shirley Slack-Smith and Corey Whisson helped RB with collections studies after the Workshop, and Bernard Metivier and Philippe Bouchet hosted us during our quest for Lamarck's venerid types in Paris (MNHN). Isabella Kappner (PEET project graduate student, FMNH) took the photograph of the Lamarck type specimens, and Lisa Kanellos (PEET project scientific illustrator, FMNH) rendered the drawings from field and laboratory sketches. Additional assistance with histochemical and photomicrographic preparation came respectively from Gloria Frischmann and Eric Chapman (MSU). Richard E. Petit, as so often before, helped with tracking down older literature. We also thank two anonymous reviewers of an earlier draft who provided constructive input. Financial support for field collecting was provided by FMNH Zoology's Department's Marshall Field Fund. Laboratory research on Veneridae was supported by U.S. National Science Foundation PEET DEB-9978119 award to RB and PMM. LITERATURE CITED Adams, H. and Adams, A. (1854-1858). The genera of Recent Mollusca; arranged according to their organization. Vol. II. John van Voorts, London. 661 pp. Allan , J. ( l 950). Australian Shells with related animals living in the sea, in freshwater and on the land. Georgian House, Melbourne. xix + 470 pp., 44 pis. Allan , J. (1959). Australian Shells with related animals living in the sea, in freshwater and on the land [revised edition]. Georgian House, Melbourne. xxi + 487 pp. , 44 pis. Angas, G.F. (1865). On the marine molluscan fauna of the province of South Australia: with a list of all the species known up to the present time; together with remarks on their habitats and distributions, etc. Part II. Proceedings of the Scientific Meetings of the Zoological Society of London 1865(43): 643- 657. Angas, G.F. (l 877). A further list of additional species of marine Mollusca to be included in the fauna of Port Jackson and the adjacent coasts of New South Wales. Proceedings of the Scientific Meetings of the Zoological Society of London 1877(13): 178- 194. Ansell , A.D. (1961 ). The functional morphology of the British species of Veneracea (Eulamellibranchia). Journal of the Marine Biological Association of the United Kingdom 41: 489- 517. Ansell , A.D. (l 962). The functional morphology of the larva, and the post-larval development of Venus striatula (Da Costa). Journal of the Marine Biological Association of the United Kingdom 42(2): 419-443.

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R. BIELER, P.M. MIKKELSEN, R.S. PREZANT