BULLETIN OF MARINE SCIENCE, 34(3): 424-434, 1984

REPRODUCTION AND DEVELOPMENT IN THE LUCINID CLAM ORBICULARIS (LINNE, 1758)

Philip Alalalo, Carl 1. Berg, Jr. and Charles N. D'Asaro

ABSTRACT The tiger lucine is a large edible clam being investigated as a mariculture candidate in the Bahamas Islands. Gonad development and spawning seasons were assessed by monthly sampling of C. orbicularis from Grand Bahama Island, Bahamas and Key Bis- cayne, Florida. Histological examination of clams showed most of the populations sampled to be ripe between April and November. Natural spawning probably occurs May to October. Codakia orbicularis is dioecious, seldom responding to standard spawning techniques, including physical and chemical stimuli. Artificial fertilization by carefully stripping gonads produced 15-20% viable embryos. Eggs are 108-112 ILm in diameter and are singularly encased in a thick capsular membrane. Following fertilization, the gastrula, trochophore and early stages develop within the capsular membrane. Upon hatching, planktonic range from 150-174 ILm in shell length and develop to the pediveliger stage in approximately 12 days at 24°C. Metamorphosis occurs approximately 16 days after fertilization. Larval development within the superfamily Lucinacea is characterized by formation of a gelatinous capsule. The long planktonic development and facultative planktotrophy of C. orbicularis is unusual for lecithotrophic bivalve larvae. Larvae of C. orbicularis and other lucinids may also derive nutrition from chemosynthetic bacteria located within their tissues, as reported for adults.

The tiger lucine Codakia orbicularis (Linne, 1758) is a large (98 mm maximum shell length) edible clam ranging from Bermuda and Florida, throughout the Caribbean and southern Gulf of Mexico, to Brazil (Abbott, 1974). Codakia or- bicularis was a staple food of the Arawak Indians, the first inhabitants of the Bahamas (Sears and Sullivan, 1978). It is harvested and eaten locally (Fischer, 1978) and is the focus of efforts considering the mariculture potential of bivalves indigenous to the Bahamas (Berg and Alatalo, 1981; 1982b). The raw meat of the clam is firm and sweet, but the gills are bitter when eaten raw. Often prepared in soups, the entire clam may be eaten after steaming. In the West Indies, C. orbicularis is found in patchy but dense assemblages, often in areas of high environmental stress (Jackson, 1972; 1973). Adult mor- phology and habitat of C. orbicularis have been reported (Allen, 1958), but most notable is their ability to live in areas of high hydrogen sulfide concentrations and to derive nutrition from chemosynthetic bacteria within their tissues (Berg and Alatalo, 1981; 1982a,b). However, no aspect of embryology or larval devel- opment has been published. Here we describe, for the first time, the reproductive biology, embryology and larval development of Codakia orbicularis.

MATERIALS AND METHODS

Specimens of C. orbicularis were collected monthly from Gold Rock Creek, Grand Bahama Island, Bahamas, and Key Biscayne, Florida, U,S.A. Gonad analysis was performed on 264 clams over a 20- month period. After preserving clams in 7% formalin/seawater, samples of gonad tissue were removed, embedded in paraffin, and sectioned at 6 ILm. Sections were stained with hematoxylin and eosin according to standard procedures (Humason, 1972), Following examination under a compound mi- croscope, gonad development was classified according to the following categories: Developing Gameles.-Male follicles are lined with spermatogonia and spermatocytes. Some sper- matids may be present in the lumen of follicles. In females, oogonia line follicles while the lumen may be filled with angular-shaped oocytes attached to follicle walls. 424 ALATALO ET AL.: REPRODUCTION IN LUCINIDCLAMS 425

Ripe Gametes.-Follicles in males contain spermatozoa with pink-staining tails filling the lumen. "Sperm balls" containing hundreds of spermatozoa joined together at the head are common. A few spermatids are present. In females nearly all eggs are oval-shaped and free in the follicle lumen. A dark-staining nucleolus is clearly visible within the nucleus of the egg. Spent or Resorbed Gametes. -Spent clams have empty follicles except for residual sperm or eggs. Sperm balls deteriorate to irregularly shaped masses of agglomerated sperm. During gamete resorption, phagocytes are always present and may completely fill the gonad. Live clams were brought to the laboratory in Woods Hole, Massachusetts, and held in unfiltered seawater at temperatures matching those at collection sites (21°-31°C). Various techniques were em- ployed to induce spawning, including thermal shock, osmotic shock and mechanical or chemical stimuli. Artificial fertilization of eggs was accomplished by carefully stripping gametes from excised bodies of ripe adult clams. Ova were collected in 8-cm diameter stacking dishes filled with filtered seawater and were fertilized with a dilute suspension of sperm. After 15 min, ova were rinsed by sieving them through 350-J.Lm Nitex screen and onto a 54-J.Lm Nitex screen. Embryos were maintained at 24°C in 2-liter Pyrex culture flasks equipped with magnetic stirrers. Since air bubbles caused veligers to stick to sides of the flask wall, magnetic stirrers were used to gently aerate cultures. After 48 h, culture flasks were removed from the stirring device and allowed to stand quietly under a light. Positively phototactic veligers swam to the surface and were slowly decanted from the flask. Veligers were maintained at 24°C in seawater passed through a 36-lLm Nitex sieve and were fed Platymonas sp. and Chlorella sp. at a concentration of I x 104 cells ml-I• Cultures were placed on magnetic stirrers and the seawater changed daily. Metamorphosed larvae were transferred to Pyrex glass trays that received slowly-flowing filtered (100 ILm) seawater. Veligers selected for sectioning were narcotized by gradual addition of a concentrated magnesium sulfate solution and embedded in paraffin using standard histological procedures. Specimens were sectioned at 8 ILm and stained with hematoxylin and eosin.

RESULTS Reproductive Development Histological analysis of Codakia orbicularis from Gold Rock Creek, Grand Bahama Island, showed ripe individuals present at each sampling date (Fig. 1). Gonad development began in spring, concurrent with rising water temperature, and was most evident during June and July. No gametogenesis was observed between December 1981 and March 1982, nor after August 1982. During 1981, half the population sampled was ripe by April, increasing to a major peak in October. In the following year, over half of the population was ripe by July and all individuals sampled were ripe in August and September 1982. Few ripe clams were found after November 1982 or December 1981 (Fig. 1). The spent stage of reproduction is reached when gonads have recently released gametes or are undergoing resorption. The percentage of spent increased dramatically in November 1981 and October 1982 following the decline in water temperature from the summer maximum. This stage predominated throughout winter. Female clams collected from the Bahamas appear to undergo rapid gonad de- velopment in early spring and remain ripe from summer through mid-fall. Male clams develop gametes later, at the beginning of summer, and are ripe by late summer. Whereas most female clams release all their gametes by late fall, male clams often remain ripe until winter. Throughout winter and spring, gonad re- sorption occurs in male clams, accompanied by deterioration of clumps of sperm. Only three hermaphrodite clams (1.2%) were found, all in February 1982. These large adults had spent gonads with residual sperm and eggs within separate follicles. No evidence of prot an dry was found in the Bahamian populations examined. The minimum size of C. orbicularis observed having follicles was 19.8-mm shell- length. One specimen, 25.4-mm long, possessed follicles undergoing gametogen- esis. Clams greater than 30 mm consistently had ripe gonads during the spawning season. 426 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, 1984

·c 30 Temperature

%

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50 25

M A AS 0 J F Months Figure 1. Gonad development of Codakia orbicularis (Linne) and seawater temperature. Gold Rock Creek, Grand Bahama Island (. = 1981;. = 1982).

Laboratory Spawning Attempts to spawn C. orbicularis in the laboratory were made between April and November using the following stimuli: rapid and gradual temperature changes, increased salinity, concentrated phytoplankton suspensions, gonad extracts, vig- orous shaking, rapid and gradual addition of hydrogen peroxide solutions and combinations of the above treatments. Results were negative. Spawning was achieved in July and October when recently collected specimens from Gold Rock Creek were placed in filtered seawater 12 to 24 h after collection. Spawning was also induced in both groups of clams by addition of 2.3 M H202 with a pH between 8.8 and 8.9. Specimens from Key Biscayne also failed to respond to the above techniques; however, ripe gametes were stripped from clams and larvae successfully reared.

Embryological Development Upon release from the gonad, ova are irregular in shape, swelling in seawater to spheres approximately 108 j.tm in diameter (Fig. 2A). The inner vitelline mem- brane is surrounded by a clear, gelatinous layer approximately 110-j.tm thick, which forms the external capsule. Further expansion of membranes results in a capsule measuring approximately 350 j.tm in diameter. Capsules of laboratory- spawned eggs are non-sticky and slightly negatively buoyant. Former attachment to the follicle is evident as a stalk connecting the vitelline membrane with the outside capsule. Sperm measure approximately 60 j.tm in length. The head is sickle-shaped, approximately 18-j.tm long and I-j.tm thick. Sperm tails range in length from 36 to 48 j.tm. Sperm are often released as sperm balls, comprised of hundreds of sperm attached at the head. Presumably, individual sperm break away from the ALATALO ET AL.: REPRODUCTION IN LUCINID CLAMS 427

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Figure 2. Codakia orbicularis. (A) Egg, 108 I'm; egg capsule, 350 I'm. (B) Early trochophore, 120 I'm. (C) Early veliger, 140 I'm. (D) Straight hinge veliger, 180 I'm. (E) Pediveliger, 190 I'm. (F) Dissoconch, 200 I'm. a-anus, aa-anterior adductor, as-apical sensory region, c-ctenidium, cg-cerebral ganglion, dg-digestive gland, gll-clear gelatinous layer, gl2-external gelatinous layer, i-intestine, m- mouth, me-mesodermal cell, p-prototroch, pa-pedal anlage, pad-posterior adductor, pg-pedal ganglion, pp-propodium, pr-pedal retractor, ra-renopericardial anlage, s-stomodeum, sc-statocyst, sg-shell gland, ss-style sac, tr-telotrochal retractor, vg-visceral ganglion, vI-velar lobe, vm-vitelline membrane, vr- velar retractor, vs-vitelline stalk. 428 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, ]984 sperm ball. Sperm swim actively upon contact with seawater, especially in the presence of eggs. During fertilization, many sperm are found attached to the outside of the ex- ternal capsule. Only about six sperm penetrate into the gelatinous layer and only one penetrates the inner vitelline membrane. Formation of first and second polar bodies occurs 30 and 90 min after fertilization, respectively. Cleavage is unequal and follows a spiral pattern. First cleavage occurs at 130 min after fertilization. Successive cleavages result in formation of a non-ciliated coeloblastula with a reduced blastocoel after 6.5 h. Epibolic gastrulation begins at 8 h, forming the primary germ layers, ectoderm and entoderm, Proliferation of ectodermal cells gives rise to a shell gland anlage. Eighteen hours later, the gastrula stage is com- pleted following invagination of the large archenteron and formation of a non- ciliated blastopore. Stomatoblasts lining the margin of the blastopore give rise to a closed stomatodeum. In the late gastrula stage, the stomatodeum invaginates first, followed by the shell gland on the dorsal surface. Within 24 h, the late gastrula differentiates into a typical trochophore larva (Fig. 2B). Major developments at this stage include evagination of the shell gland, formation ofthe prototroch, and expansion ofthe apical plate. In the early trocho- phore, the tip of the invaginated shell gland extends farther anteriorly than the corresponding part of the stomodeum. Slowly the shell gland evaginates below the band of long cilia which form the prototroch. During trochophore develop- ment, differentiation of primary mesodermal, mesenchymal, and endodermal organs begins. A pair of proto nephridia and the renopericardial anlage arise from mesodermal mother cells. Larval retractor muscle anlagen develop from mes- enchymal cells. The digestive anlage, endodermal in origin, begins to separate into a compound stomach region and a pair of rudimentary lateral, digestive glands. The early trochophore is about 120-~m long and rotates in an anterior direction within the egg capsule, using long cilia of the prototroch. By 40 h after fertilization, most trochophores have developed to the early veliger stage (Fig. 2C). The first larval shell, prodissoconch I, is presumably secreted by the evaginated shell gland and is about 140-~m long. From the prototroch a velum forms, with an anterior ciliary band for food collection and locomotion and a posterior band of cilia for transporting food. The mouth and anus form and are found connected to the archenteron. Ciliated epithelial cells are found scattered within the mouth and anus. The digestive glands have expanded and contain much of the primary yolk in large vacuolated cells. Formation of the nervous system commences 50 h after fertilization. Prolif- eration of ectoderm in the pedal anlage forms the pedal ganglia. Although the origin of the pleural ganglia is not apparent, pleural ganglia in other Lamelli- branchia arise from ectoderm of the body wall (Raven, 1966). Pleural ganglia later fuse with cerebral ganglia to produce the complex cerebropleural ganglion. This ganglion attaches to the sensory area of the apical plate. The germ-layer origin of musculature is difficult to trace. However, three pairs of velar retractors, one pair of pedal retractors and two pairs of teletrochal re- tractors appear to form from mesenchyme cells. The anlage of the anterior ad- ductor consolidates and becomes functional when the primary larval shell is complete. Prior to hatching, the gelatinous egg capsule has been eroding such that contact by the larva produces considerable distortion of the membrane. By the third day after fertilization, the velum is well developed and resultant velar activity tears the capsule wall, releasing the veliger (Fig. 2D). While prodissoconch II, the second shelled stage forms by deposition of shell at the mantle edge (Carriker and Palmer, ALATALO ET AL.: REPRODUCTION IN LUCINID CLAMS 429

1979), the prodissoconch I/prodissoconch II boundary may indicate the point at which valve closure is complete in the developing larva (Waller, 1981). Although no direct observation of valve closure in C. orbicularis was made, the velum completely retracts into the mantle cavity, suggesting complete closure. At hatch- ing, larval shells range in length from 174 J.Lm to 180 J.Lm and are transparent, unsculptured, and wider at the anterior end. Shell growth of C. orbicularis is negligible up to the pediveliger stage. Internally, the stomach undergoes division, forming gastric and style sac stom- achs with the latter associated crystalline style. The lumen of each digestive gland arises as a large evagination of the stomach wall. Additional muscle fibers make up the crescent-shaped anterior adductor. A rudiment of the posterior adductor forms anterior to the anus. Neural connectives develop, joining the cerebral and pedal ganglia and the visceral and pedal ganglia together. A pair ofstatocysts arise from ectodermal invaginations dorsal and lateral to the pedal ganglia. Although C. orbicularis larvae are positively phototactic, a light-sensitive organ was not found. By the fifth day, gastric shield, crystalline style, and typhlosoles are fully formed in the style sac stomach. The intestine loops dorsally into the blastocoelic cavity where elements of the definitive renopericardium develop. Formation of the larval digestive glands and rectum is completed at this time. Two major developments occur by the eighth day. First, the pedal anlage elon- gates ventrally, forming the propodium, which is ciliated on the ventral side. Secondly, as a result of the dorsal shift of the digestive tract, the intestine coils anteriorly within the blastocoel cavity. There is also a decrease in size of the storage cells located in the digestive gland, indicating further reduction of stored embryonic food. Lateral to the visceral ganglia, at the junction of the mantle and body wall, a pair of ctenidial anlagen form. Most larvae drop from the and become crawling pediveligers 12 days after fertilization (Fig. 2E). Shell length of prodissoconch II has increased to only 190 J.Lm since hatching. Larvae use the prominent propodium to creep along the bottom, and while swimming, often keep it wrapped around one valve. During this stage, the velum decreases in size and is often withdrawn when the pediveliger is crawling. Velar reduction is accompanied by gradual disappearance of velar retractors and large vacuolated cells in the velum. Pedal retractors become in- corporated into the foot and body wall. At the same time, anterior and posterior adductor muscles increase in size and become more definitive. Rudimentary siphons develop by fusion of the mantle lip near the posterior adductor muscle. Development of the digestive tract continues as the digestive gland expands around and fuses with the anterior stomach and esophagus. Prior to development of gills, the kidney and pericardial vesicles separate, and veins and arteries begin to form. The major pedal sinus opens close to kidney vesicles, each of which is associated with the edge of a ctenidial fold. Two lateral folds form in each ctenidia anlage and become lined with metachronal cilia. Bands of cilia appear on anterior edges of each ctenidium. As growth progresses, the anterior ctenidium in each pair becomes larger. Nearly all C. orbicularis larvae complete metamorphosis by the 16th day. No special substrata are required. During metamorphosis, the remaining velar rem- nants are shed. Anterior ciliary bands associated with the ctenidia connect with the complex oral and palp cilia located in the mouth region. Eventually the posterior lip of each ctenidium links with the anterior lip of the mouth. The digestive gland continues to expand into the foot region, surrounding the style sac stomach. With reduction of cerebropleural ganglia, the pedal and visceral ganglia are now the most prominent organs of the nervous system. 430 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, 1984

Metamorphosis in bivalve molluscs is characterized by the formation of the dissoconch or post larval shell. The earliest dissoconch of C. orbicularis is ap- proximately 200 ~m in length, possessing distinct growth rings, but no prominent umbones. Shell growth is rapid, particularly in coarsely filtered seawater. Although no byssal gland is present, juvenile clams do not burrow, even when presented with fine-grained substrata from natural C. orbicularis habitat. Instead, juvenile clams crawl continuously over various substrata, rarely stopping for more than a few minutes. Only a posterior exhalent siphon is formed by fusion of the mantle lip. Although the primary exhalent siphon is hardly extensible, this structure can be extended six times the length ofthe shell in adult clams (Allen, 1958). Eighteen days after fertilization, juvenile C. orbicularis are 224- to 250-~m long and possess complete digestive, nervous, circulatory, and excretory systems (Fig. 2F).

DISCUSSION Gamete Development Tropical bivalves may spawn continuously or may exhibit one or more peaks of spawning (Sastry, 1979). The breeding season is often extended in the tropics, and sexually mature individuals are commonly found year-round (Moore and Lopez, 1972; 1975). Monthly sampling of Codakia orbicularis from Gold Rock Creek showed over 75% of the population was ripe in October 1981 and all were ripe from August to September the following year. While at least a few ripe individuals were found at all sampling times, natural spawning probably occurs between May and October, possibly triggered by a decline in water temperature from the summer maximum (Fig. 1). Ripe gametes were obtained from clams collected at Key Biscayne from May to September. Induction of spawning in the laboratory was successful only between July and October. The population at Gold Rock Creek undergoes gametogenesis over a long period of time; however, individual maturation occurs relatively quickly. Female clams from Gold Rock Creek matured during spring, while males matured throughout summer. The percentage of spent individuals greatly increased in November and remained high through April 1982. Gonad resorption was prevalent in male clams throughout winter and spring. Retention of sperm is common in C. orbicularis, suggesting that male clams spawn only after female gametes are detected. In addition, male clams may only spawn a portion of their gametes, whereas female clams appear to empty the entire gonad. Sperm balls have been reported in oysters, Ostrea edulis (Orton, 1927; Loosanoff, 1962) and 0. lurida (Coe, 1931), and the clam, Corbicula cf.jluminalis (Morton, 1982). Spermatozoa form large morulae in C. cf. jluminalis and are probably released intact during spawning. Embryological Development Ockelmann (1965) redefined Thorson's earlier (1950) classification of larval types into three main types of development: planktotrophic, lecithotrophic and direct. Planktotrophic development is characterized by a small egg, a small pro- dissoconch I and a planktonic feeding stage that could last up to 6 weeks. The larva typically shows a marked change in size and shape. Lecithotrophic larvae hatch from intermediate-sized eggs, form an intermediate-sized prodissoconch I, and are planktonic for only a short period, never more than a few days. Nutrition is derived from egg reserves. Little growth occurs between hatching and meta- morphosis. Lecithotrophic larvae having no planktonic larval stage and usually hatching as benthic juveniles exhibit direct development. Eggs are large as are the embryonic shells. Direct development often involves brood protection. ALATALO ET AL.: REPRODUcrION IN LUCINID CLAMS 431

Codakia orbicularis exhibits several features characteristic of lecithotrophic development (Table I). First, C. orbicularis spawns eggs that are within the 90- 140 ~m range proposed by Ockelmann (1965) for lecithotrophic development. Secondly, prodissoconch I is 140-174 ~m, within the characteristic lecithotrophic range of 135-230 ~m. Finally, growth is minimal during the planktonic stage of development. However, Codakia orbicularis spawns many thousands of eggs (Alatalo, pers. comm.), typical of species exhibiting planktotrophic development (Thorson, 1946). After hatching from the capsule, a 10-day planktonic stage ensues, characteristic of planktotrophic development. Although phytoplankton have been observed in the digestive tract, recent studies show that development rates of fed and non- fed C. orbicularis larvae are similar (Berg and Alatalo, 1982a). Facultative plank- totrophy may apply to some gastropod species, but conclusive reports are scarce (Williams, 1980; Jablonski and Lutz, 1983). The only reported account of plank- totrophy by a lecithotrophic larval bivalve is that of Allen (1961) concerning possible feeding in Pandora inaequivalvis prior to metamorphosis. In his review of bivalve larval development types, Chanley (1968) emphasized the influence of incubation on modifying basic larval types. External incubation in the form of a gelatinous membrane surrounding the egg has been reported for bivalve molluscs exhibiting all three development types. Generally the nature of the capsule, the duration of encapsulation, and the development stage at hatching differ among species (Table 1). Cerastoderma edule hatches from a galatinous capsule as a young veliger and undergoes a 3-week planktotrophic stage (LeBour, 1938; Creek, 1960). The gelatinous capsule seldom lasts beyond the blastula stage of Mercenaria mercenaria whose larvae feed for up to 2 weeks in the plankton (Loosanoffand Davis, 1950). Lecithotrophic development with a short planktonic stage is found in the primitive Paleotaxodont bivalves, Nucula proxima and Yoldia limatula, which develop within a ciliated test that is shed at metamorphosis (Drew, 1897; 1899). Pandoracean larvae such as Pandora inaequivalvis, Lyonsia hyalina, and Entodesma cuneata hatch from their capsules as trochophores and undergo a short planktonic stage before metamorphosis (Allen, 1961; Chanley and Castagna, 1966; Campos and Ramorino, 1981). Astarte castenea develops directly within its capsule, hatching in 22-26 days after fertilization (Goodsell and Lutz, in press). Larval development within the superfamily Lucinacea may be lecithotrophic or direct, but is characterized by the formation of a gelatinous capsule. Loripes lucinalis (=Lucina lactea), family Lucinidae, spawns encapsulated eggs that adhere together and develop extremely slowly (Pelseneer, 1926). Loripes psidium (Table I) hatches as a trochophore in 15 h and is planktonic for 30 days (Sang, 1954). Codakia costata and Lucina nassula from the Bahamas spawn small eggs indi- vidually encased in large gelatinous capsules (Alatalo, pers. comm.). Blacknell and Ansell (1974) report that Thyasira gouldi (Table 1), family Thyassiridae, develops directly from a demersal capsule after an extremely long development period of 36-51 days at 10°-16°C. Other members of this family, Thyasirajlexuosa and T. sarsi, develop lecithotrophically (Ockelmann, 1965). Encapsulation of early developmental stages followed by the release of free- swimming, pre-metamorphic larvae is termed "mixed development" (Pechenik, 1979). The gelatinous capsule is presumed to protect the egg and developing embryo from predators, disease, and environmental stresses. Ockelmann (1958) speculates that non-adhesive membranes provide support for floating eggs or act as an additional food supply. Pechenik (1979), however, suggests that the major benefit of mixed development is to reduce mortality of small, unshelled embryos 432 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, 1984

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...: ALATALO ET AL.: REPRODUCTION IN LUCINID CLAMS 433 in the plankton. Large numbers of immobile sperm attached to the capsule during fertilization also suggest an effective mechanism preventing polyspermy (Allen, 1961). Development in C. orbicularis may be described as lecithotrophic with a long planktonic stage. While a long planktonic stage aids in dispersal, mixed devel- opment together with facultative planktotrophy may represent adaptations for planktonic survival in tropical seas where phytoplankton are typically sparse. Furthermore, the possibility exists that C. orbicularis larvae obtain nutrition through intracellular chemoautotrophic bacteria within their tissues as hypothe- sized for the adults (Berg et aI., 1983; Berg and Alatalo, 1982a). The devel- opmental stage at which bacterial transmission occurs is unknown. Iflarvae derive nutrition from chemosynthetic bacteria, a new class oflarval nutrition is necessary: chemoautotrophic to complement the categories of planktotrophic and lecithotro- phic development. In nature, Codakia orbicularis is likely to rely on all three types of nutritional pathways during its development. Larvae of other species of chemoautotrophs such as the deep-sea clam Calyptogena magnifica may rely more on chemoau- totrophy.

ACKNOWLEDGMENTS

The authors gratefully thank N. Adams, E. Beale, G. Waugh, and G. Woon for technical assistance during this study. Dr. H. B. Michel, University of Miami, provided laboratory facilities and useful suggestions to D' Asaro. M. Castagna and R. Prezant kindly reviewed the manuscript. This research was supported in part by a grant from the Wallace Groves Aquaculture Foundation, Freeport, Bahamas.

LITERATURE CITED

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DATEACCEPTED: September 19, 1983.

ADDRESSES:(P.A. and CJ.B .. Jr.) Marine Biological Laboratory. Woods Hole, Massachusetts 02543; (CN.D.) Department of Biology. University of West Florida. Pensacola. Florida 32504.