Roxanna Smolowitz Aquatic Diagnostic Laboratory, Roger Williams University, Bristol, RI, USA Bivalvia (Lamellibranchiata, Pelecypoda) is a large class of laterally compressed animals characterized by two calcified variably flattened to deeply cupped valves (which make up the shell) that are attached to each other at the dorsal surface with teeth (interlocking waves in the calcified shell, not true teeth) spanned by a flexible hinge ligament. The inner surfaces of the valves are lined by a thin mantle. The visceral mass (body) of the bivalve extends from the dorsal attachment into the space (pallial cavity/mantle cavity) between the mantle‐lined valves. There are more than 15 000 species of bivalves, most of which are marine. Because they are filter feeders, most species live on or in the sediment, or on rocky surfaces of relatively shallow microalgal rich marine or fresh waters. Based on their overall morphology, they are separated into five subclasses but are practically placed into the following groups: clams, cockles, mussels, scallops, and oysters. In the past, bivalves were an important human (and animal) food source. Importantly, bivalves are widely recognized as providing an ecosystem service as filter feeders by removing suspended material from the water column and either incorporating it into their bodies or depositing undigested materials on the sediment surface in mucus‐bound composites. A single bivalve can filter between 1 and 4 L/h and calculations based on oyster populations in 1880 have determined that it only took 3.3 days to filter all of the water in the Chesapeake Bay (Rice 2001). Today in many areas, bivalves, especially those species used as food by people, have either been fished heavily and/or have suffered from diseases, resulting in significant decreases in their populations. While wild capture is still commonly used for many species of edible bivalves, aquaculture was, and continues to be, a method of producing bivalves for human consumption. The species of bivalve that are routinely cultured varies by country and climate, but the most commonly cultured bivalves are oysters (Crassostrea virginica, the eastern oyster and Crassostrea gigas, the pacific oyster), clams (Mercenaria mercenaria, the northern clam, Venerupis philippinarum, the Manila clam and Ruditapes decussatus, the grooved carpet clam), mussels (Mytilus edulis, the blue mussel and Mytilus galloprovincialis, the Mediterranean mussel), the Yesso scallop (Patinopecten yessoensis), and the common cockle (Cerastoderma edule). As an example of the increased importance of aquaculture, the global production of Pacific oysters increased from 149 163 tons in 1950 to 625 925 tons in 2014 (FAO fact sheet; www.fao.org/fishery/species/3514/en). Bivalve larvae are amazingly similar from fertilization until metamorphosis which makes learning larval anatomy easy, but identification of larvae from different species difficult when samples are collected from the wild environment! Recently developed molecular identification methods are helping in that effort (Lutz et al. 2018). The stages of development prior to metamorphosis are (in order of development): fertilized egg, trophophore, Prodissiconch I (D‐shaped larvae) (Figure 6.1) and Prodissiconch II. The Prodissiconch II stage is subdivided into early and late stages named sequentially umbo (Figure 6.2) and pediveliger stages (Figures 6.3 and 6.4). Once a larva becomes a fully developed pediveliger, it searches for an appropriate location to attach using small protein threads (byssal threads) extruded by a gland in the foot. In the Prodissoconch I and II stages (Carriker 2001; Elston 1980; Galtsoff 1964; Morse and Zardus 1997; Tompson et al. 1996), the velum (consisting of two circular lobes, one inside the other, that are covered with rows of cilia and are adjacent to the mouth) is used both for movement in the water column and to filter feed. Both anterior and posterior adductor muscles, as well as velar retractor muscles, can be identified in pediveligers. The velum and soft tissues can be retracted into the thin translucent shell by the retractor muscles when startled. The esophagus is located adjacent to the posterior portion of the velum, is also heavily ciliated, and funnels food to the stomach. Figure 6.1 D‐shaped eastern oyster (Crassostrea virginica) larvae. Figure 6.2 Early Prodissoconch II (umbo) stage of the eastern oyster. a, stomach lumen; b, esophagus; c, retracted velum; d, digestive gland cells; e, style sac; f, anterior adductor muscle. In the Prodissoconch II stage, histologically, just ventral to the velum is a focus of distinct but undifferentiated cells referred to as a cerebral ganglion. The digestive gland, and its finely vacuolated absorptive cells, is prominent in the more developed larvae and is located around the stomach and esophagus. In Prodissoconch II larvae, the style sac and intestine can also be located extending from the stomach lumen. In the pediveliger stage of development, a rudimentary foot containing a byssal gland and rudimentary gills can be identified projecting into the pallial (mantle) cavity. The gills develop from the mantle tissue lining the inner surface of the valves (see descriptions of the mantle and mantle cavity in adult anatomy). At the pediveliger stage, paired statocysts appear with the body mass. These organs are formed by invagination of the ectoderm and are connected by a fine tube that empties into the mantle cavity surrounding the body. The statocysts are composed of two cell types: a nonciliated cell, which produces the thin translucent statoliths, and a strongly ciliated cell type with cilia that extend into the lumen of the statocyst. Processes from the ciliated cells form a nerve that connects to the pedal ganglia (Cragg and Nott 1977). Research demonstrates that statocysts are gravity receptors. Statocysts are retained in adult animals after metamorphosis in some species. Figure 6.3 Pediveligers of hard clams (Mercenaria mercenaria). Arrows indicate eyes. In late‐stage Prodissoconch II (pediveliger), a pair of pigmented eyespots develop on the budding gill tissue (see Figure 6.3). The eyespots consist of a cell with pigmented granules that can be seen through the thin, translucent valves. It is thought the eyes provide directional photoreception (Cragg 2016). Aquaculturists often use the term “eyed up” to indicate the age of the larvae. After attachment, the larvae undergo metamorphosis (also termed setting). At metamorphosis, depending on the species, some larval organs are destroyed and others are formed. Clams, cockles, and mussels undergo the least amount of change. At metamorphosis, clams lose the velum, and slightly rearrange the organs so that the mouth is anterior and the rectum posterior with gills suspended from the dorsal portions of the soft body in an anterior to posterior direction. Oysters undergo the most dramatic rearrangement of tissues and organs. They lose not only the velum but also the foot and the anterior adductor muscle. The mouth moves dorsally to a location just underneath the ligament, resulting in a J shape to the gills. Scallops also dramatically change. They lose the anterior adductor muscle and reorient organs to form a distinct kidney, gonad, and a C‐shaped gill. Figure 6.4 Diagram of a pediveliger of the European flat oyster (Ostrea edulis). a, anus; abc, aboral belt of cilia; ant.ad., anterior adductor muscle; a.p.o., apical sense organ and ganglion; b.g., byssus gland; cr.s, crystalline style sac; d.div, digestive diverticula; e., esophagus; ey., eye; f., foot; f.r., foot retractor muscles; g, gill rudiment; g.sh., gastric shield; h.r., heart and kidney rudiment; int., intestine; m., mouth; m.c., mantle cavity; p.g., pedal ganglion; post.ad, posterior adductor muscle; r., rectum; r.v., velar retractor muscles; st., stomach; stc., statocyst; v., velum; v.g., visceral ganglion. Source: Galtsoff (1964). Post metamorphosis (even though often no larger than 450 μm in diameter!), bivalves take on the morphologic appearance identified for each subclass of bivalve as described above. In this work, we will discuss the anatomy of the clam (which changes the least at metamorphosis) (Eble 2001) and then describe important anatomic differences in oysters, scallops, mussels, and cockles (Benninger and Le Pennec 2016; Eble 2001; Eble and Scro 1996; Morton 2008). Anterior, posterior, dorsal, and ventral directions can be identified in clams (Figure 6.5) (Gosling 2003; Elston 1980). Dorsal, embryologically, is the area where the valves connect via the shell ligament and interlocking teeth (Figure 6.6). The connected valves together are termed a shell. The ligament is primarily composed of a firm to hard, black/brown laminated “resilium” that is secreted by the mantle and composed of elastic organic material. The resilium holds the two valves together but also acts to open the shell valves when adductor muscles are relaxed (Carriker 1996; Galtsoff 1964). Figure 6.5 A hard clam with labeled directions. a, dorsal; b, posterior; c, ventral; d, anterior. Figure 6.6 Fixed, shucked hard clam (left demibranchs and a portion of the visceral mass have been removed). Adductor muscle consisting of a, catch muscle and b, quick muscle. Other organs are: c, mantle edge; d, siphon; e, pericardial sac; f, gonadal and intestinal loop in visceral mass; g, teeth; h, digestive gland; i, palps. Figure 6.7 Diagram of an Atlantic surf clam (Spicula solidissima) with left valve and gill removed. AA, anterior adductor muscle; An, anus; Au, auricle; CG, cerebral ganglion; ED, excurrent siphon; Fo, foot; Gi, gill; Go, gonad; Ki, kidney; ILP, inner labial palp; In, intestine; IS, incurrent siphon; Mo, mouth; OLP, outer labial palp; Pa, posterior adductor muscle; PG, pedal ganglion; SS, style sac; St, stomach; Ve, ventricle; VG, visceral ganglion. Source: Morse and Zardus (1997). Reproduced with permission from John Wiley & Sons. Bivalves lack a head but the mouth area is considered anterior. The rectum empties into the posterior area (Figure 6.7). In most adult bivalves, when examining the closed animals (valves shut tight), some portion of the outer surface of the shell hinge or adjacent phalanges extends in an anterior direction (see Figure 6.5). Clams have both an anterior and posterior adductor muscle. While the interlocking teeth and hinge ligament hold the two valves of the shell together dorsally, it is the adductor muscles extending from the left valve to the right valve that close the shell (a fatigable action!). Extending from the dorsum of the shell on the inner surface of both valves is the mantle. This easily disregarded organ is responsible for production of the entire shell and the ligament. The mantle is divided into two portions: the thin membranous mantle (pallial mantle) that lines the inner surface of the valves and the mantle edge (mantle border), a thickening of the mantle that occurs along the outer circumference adjacent to the edges of the valves. The mantle is lightly connected to the inner surface of the shell from the dorsal ligament to the crescent‐shaped pallial line which can be found from 1 mm to 3 cm (depending on species and size of animal) from the valve edge on the inner surface of the valve. It parallels the curvature of the valves except in the location of the siphon. From the pallial line to the edge of the shell, the mantle is detached from the inner surface of the valve and can either be extended over the edge of the valve or retracted into the closed shell. In some clam species, the mantle edge is fused along much of the circumference, leaving only a small opening for the foot. In these animals, the mantle cannot be fully retracted into the shell. Posteriorly, the mantle is fused in all clams and is modified to form a siphon, which may or may not be fully retractable, depending on the species. The visceral mass contains most of the organs, including the foot, and extends from the dorsum into the mantle cavity (pallial cavity) of the shell. Laterally, on both sides of the visceral mass and attached at the dorsum between the mantle and the visceral mass, are two demibranches of longitudinally oriented gills. The siphon, a specialized area of the posterior mantle, is divided into two channels. The incurrent siphon (ventral to the excurrent siphon) is used to draw water into the mantle cavity, and the excurrent siphon eliminates water from the mantle cavity. Water (fresh or salt) enters the mantle cavity, flows over the gills and through small ostia (holes) in the surface of the gill. The water flows up the water tubules inside each of the lamellae of the gills (demibranchs) toward the dorsum of the clam where vertical water tubules empty into large, horizontally oriented, dorsal water tubules. The water then flows through the dorsal tubule posteriorly to the excurrent siphon where it is eliminated from an animal’s mantle/gill cavities (Figure 6.8) (Pearse et al. 1987). While it appears that water is flowing through the gill and body tissues, it is really flowing through tubules surrounded by gill and body tissues. It does not enter the body tissues (structure of the gills is described under histology). Almost all bivalves are filter feeders and directed water flow provides a way to expose the surface of the gills (where particulate matter is gathered) to a continuous source of particulate (food, etc.)‐containing water. Figure 6.8 Diagram illustrating the direction of water flow from the mantle cavity through the gill to the dorsal gill passage. The anterior of the clam has been removed. The ostia (pores) of the gills are microscopic in live tissue and are enlarged here for illustrative purposes. Source: Pearse et al. (1987). Reproduced with permission from John Wiley & Sons. Figure 6.9 Intact eastern oyster. a, anterior (ligament); b, dorsal. The surface of the visceral mass is smooth to wrinkled and the visceral mass itself, depending on the reproductive stage (or disease), will be firm and thick to thin and edematous. Within the visceral mass are found the gastrointestinal tract, the reproductive tract, excretory organs, most of the cardiovascular system, the neural system, and abundant variously oriented muscles. Post metamorphosis (as noted above), the oyster’s orientation is much different from that of other bivalves (Figure 6.9). The shell ligament becomes anterior and the ventral surface of the shell becomes posterior. Dorsal is now what would have been anterior in the larvae and only a posterior adductor muscle remains. Along the length of the oyster, both sides of the mantle fuse with the dorsum of the gills. The fusion extends past the posterior adductor muscle area to the mantle edge and is strongly adhered to the inner surface of the valves (Figure 6.10). Thus the mantle cavity is divided into two major sections, the hypobranchial chamber containing the gills and the epibranchial chamber (dorsal chamber) containing most of the visceral mass. Oysters do not have a foot. Instead, the inner surfaces of the gill lamellae (demibranchs) are directly adjacent to each other. Oysters also do not have siphons. In oysters, water enters the mantle cavity, flows into the ostia and travels dorsally up the tubules in the gill. Instead of emptying into dorsal water tubules, the water flows through a sieve‐like structure located at the fusion of the mantles and gills and into the epibranchial chamber, where it is flushed out of the cavity by action of the adductor muscle opening and closing the valves (Figure 6.11). Figure 6.10 Shucked eastern oyster. a, digestive gland; b, pericardial sac with heart; c, translucent portion of adductor muscle; d, area of posterior mantle fusion forming the epibranchial (dorsal) chamber (e) and hypobranchial chamber (ventral) (f). Figure 6.11 Diagram of an oyster showing the opening of the gill’s water tubules into the epibranchial chamber (composed of the promyal and cloacal chambers). ad.m, adductor muscle; cl, cloaca; f, fusion of the mantle lobes and gills; pr.ch., promyal chamber; r, rectum. Source: Galtsoff (1964). Figure 6.12 Shucked Atlantic sea scallop (Placopecten magellanicus), fixed in formalin. a, portion of the left gill (right gill removed); b, foot; c, palp; d, lips; e, digestive gland; f, pericardial sac; g, quick portion of the adductor muscle; h, catch portion of the adductor muscle; i, rectum; j, kidney; k, gonad; l, scallop eye. Post metamorphosis, only the large posterior adductor muscle remains in scallops (Figures 6.12 and 6.13). It is in a central location in the midportion of the shell. The foot also remains but is very small and is located just ventral to the mouth and palps. The visceral mass is expanded and most of the mass is located anterior to the adductor muscle. There are no siphons, but ciliary action of the cells lining the mantle cavity creates directed flow from the anterior “wings” adjacent to the ligament of the dorsal scallop shell to the posterior wings of the shell. Mussels are very similar to clams, but they are the most dorsal‐ventrally compressed and anterior‐posteriorly elongated of all the bivalves. Their mantles are sealed along most of the length of the valves. Small siphons extend from the posterior portion of the sealed mantle. About one‐third of the way from the anterior end, the mantles are not sealed so that the foot can be extended through the gap to provide movement and access for byssal thread attachment (see section 6.3.9.2 for further detail on byssal thread). Figure 6.13 Diagram of a pink scallop (Chlamys hastata) with left valve and gill removed. An, anus; Au, auricle; BT, byssal threads; DD, digestive gland; Fo, foot; Gi, gill; Go, gonad; In, intestine; Ki, kidney; Li, peribuccal lips; PA, posterior adductor muscle; PGl, pericardial glands; SS, style sac; St, stomach; Ve, ventricle. Source: Morse and Zardus (1997). Reproduced with permission from John Wiley & Sons. In all bivalves, the gills function as a food collection organ as well as for respiration. Food is collected by ciliated cells on the surface of the gills. On the gill surface, the particulate matter is mixed with mucus and transported by directed ciliary motion to the ventral food groove of the gills. Mucus balls of food are moved along the food groove/canal to the palp/mouth complex. Bilaterally from either side of the mouth and extending into the mantle cavity are the palps (the mouth is small in size and usually cannot be seen grossly). The palps (thought to be highly sensory) break up the food‐containing mucus balls, sort through the material and select appropriate food particles that are then transferred to the mouth. Nonfood particles are moved to the inner surface of the membranous mantle (usually adjacent to the incurrent siphon or a similar position in animals without siphons). Periodically, these nonfood particles, which can be seen grossly and are termed pseudofeces, are “burped” out through the incurrent siphon or are flushed out of the shell. In clams, palps are long oar‐like structures that extend into the mantle cavity. The outer set of palps attach to the body above the mouth and the inner set attach below the mouth. The structure of the palps varies greatly between different types of bivalves. Oysters show a similar orientation of the palps, but they are much shorter and form small triangular flaps around the mouth. In scallops, the palps connect to the dorsally and ventrally oriented cauliflower‐like lips. Scallop lips are especially unusual and are discussed further in the histology section. Food particles enter the mouth, and move through the esophagus and into the stomach. The stomach is a thin‐walled, irregular structure divided into two major compartments. Major ducts lead from the anterior compartment of the stomach into the digestive gland (where most digestion and absorption occur). Projecting into the posterior portion of the stomach is the style, a crystalline structure made of mucin‐type glycoproteins that are continually produced by the epithelium of the blind‐ended style sac. The jelly‐like style can be grossly dissected out from the surrounding tissue. The projecting end of the style rotates against a gastric shield composed of chitin (a firm plaque on the dorsal surface of the stomach) that is located on the opposite side of the stomach lumen from the style sac. The two structures produce a mortar and pestle‐like action that breaks down food particles. The digestive gland, usually colored brown/black, surrounds the stomach on its ventral and lateral sides. Exiting from the posterior stomach is the descending intestine, which winds ventrally through the visceral mass then ascends to become the rectum. The rectum extends dorsally and posteriorly, enters into the pericardial coelom and, in clams, continues through the center of the heart’s ventricle to become the rectum. The rectum leaves the heart and continues in a dorsal positon adjacent to the posterior aorta (and the aortic bulb, to be discussed later) where it exits the pericardial coelom and extends to a location dorsal to the posterior adductor muscle. The anus deposits feces in the excurrent siphon lumen. In oysters, the rectum is attached to and/or is bilaterally surrounded by the dorsal side of the ventricle and the rectum deposits feces in the cloacal chamber (a posterior portion of the epibranchial chamber) on the dorsal side of the mantle fusion (as discussed previously). In scallops, the rectum curves from dorsal to ventral around the adductor muscle and empties into the posterior ventral mantle cavity. Bivalves have an open circulatory system. Bivalve “blood” is termed hemolymph. In bivalves, the heart consists of large right and left atria with poorly organized, thin muscle bundles that receive hemolymph from thin‐walled veins. Atria empty into a single ventricle composed of thick trabeculated muscle bundles. An anterior aorta leaves the ventricle, divides and supplies the gill and anterior organs. A posterior aorta leaves the ventricle and supplies the posterior adductor muscle and siphon. Before leaving the pericardial coelom, the posterior aorta forms a muscular aortic bulb. The bulb is spongy and can contain large amounts of hemolymph. The bulb is thought to allow space for the “back‐flushing” of hemolymph that occurs when the siphons contract in clams. The bulb is often not present in bivalves without siphons. The aortas and larger arteries distribute hemolymph to the body. Arterioles empty into sinusoids which surround and permeate the tissues. Hemolymph flows through the sinusoids and is carried back to the atria through large and poorly delineated veins. The bivalve excretory system is divided into two parts and is unusual in that the pericardial sac and the atria are part of the system. Pericardial glands, which extend from the pericardial wall or are an extension of the atrial surface (often termed a green gland when see grossly), can be located between the pericardial sac and the dorsal ligament. In clams, the second grossly visual portion of the kidney, a thin brown tissue, underlies the pericardial sac. In oysters, it is not possible to see the second part of the kidney grossly. C‐shaped, brown kidney tissues in scallops are prominently located between the anterior surface of the adductor muscle and the gonad tissues.
6
Mollusca: Bivalvia
6.1 Introduction
6.2 Gross Anatomy
6.2.1 Larval Morphology
6.2.2 Adult Bivalve Gross Morphology
6.2.2.1 General Body Plan Post Metamorphosis
6.2.2.2 Gastrointestinal System
6.2.2.3 Circulatory System
6.2.2.4 Excretory System
6.2.2.5 Reproductive System
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