Bivalvia Temporal range: Early Cambrian – recent[1][2] PreꞒ Ꞓ O S D C P T J K Pg N
"Acephala", from Ernst Haeckel's Kunstformen der Natur (1904)
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Phylum:	Mollusca
Class:	Bivalvia Linnaeus, 1758
Subclasses
Heterodonta Palaeoheterodonta Protobranchia Pteriomorphia And see text

Bivalvia (/baɪˈvælviə/), in previous centuries referred to as the Lamellibranchiata and Pelecypoda, is a class of marine and freshwater molluscs that have laterally compressed bodies enclosed by a shell consisting of two hinged parts. As a group, bivalves have no head and they lack some usual molluscan organs, like the radula and the odontophore. The class includes the clams, oysters, cockles, mussels, scallops, and numerous other families that live in saltwater, as well as a number of families that live in freshwater. The majority are filter feeders. The gills have evolved into ctenidia, specialised organs for feeding and breathing. Most bivalves bury themselves in sediment, where they are relatively safe from predation. Others lie on the sea floor or attach themselves to rocks or other hard surfaces. Some bivalves, such as the scallops and file shells, can swim. Shipworms bore into wood, clay, or stone and live inside these substances.

The shell of a bivalve is composed of calcium carbonate, and consists of two, usually similar, parts called valves. These valves are for feeding and for disposal of waste. These are joined together along one edge (the hinge line) by a flexible ligament that, usually in conjunction with interlocking "teeth" on each of the valves, forms the hinge. This arrangement allows the shell to be opened and closed without the two halves detaching. The shell is typically bilaterally symmetrical, with the hinge lying in the sagittal plane. Adult shell sizes of bivalves vary from fractions of a millimetre to over a metre in length, but the majority of species do not exceed 10 cm (4 in).

Bivalves have long been a part of the diet of coastal and riparian human populations. Oysters were cultured in ponds by the Romans, and mariculture has more recently become an important source of bivalves for food. Modern knowledge of molluscan reproductive cycles has led to the development of hatcheries and new culture techniques. A better understanding of the potential hazards of eating raw or undercooked shellfish has led to improved storage and processing. Pearl oysters (the common name of two very different families in salt water and fresh water) are the most common source of natural pearls. The shells of bivalves are used in craftwork, and the manufacture of jewellery and buttons. Bivalves have also been used in the biocontrol of pollution.

Bivalves appear in the fossil record first in the early Cambrian more than 500 million years ago. The total number of known living species is about 9,200. These species are placed within 1,260 genera and 106 families. Marine bivalves (including brackish water and estuarine species) represent about 8,000 species, combined in four subclasses and 99 families with 1,100 genera. The largest recent marine families are the Veneridae, with more than 680 species and the Tellinidae and Lucinidae, each with over 500 species. The freshwater bivalves include seven families, the largest of which are the Unionidae, with about 700 species.

Etymology

The taxonomic term Bivalvia was first used by Linnaeus in the 10th edition of his Systema Naturae in 1758 to refer to animals having shells composed of two valves.^[3] More recently, the class was known as Pelecypoda, meaning "axe-foot" (based on the shape of the foot of the animal when extended).

The name "bivalve" is derived from the Latin bis, meaning "two", and valvae, meaning "leaves of a door".^[4] ("Leaf" is an older word for the main, movable part of a door. We normally consider this the door itself.) Paired shells have evolved independently several times among animals that are not bivalves; other animals with paired valves include certain gastropods (small sea snails in the family Juliidae),^[5] members of the phylum Brachiopoda^[6] and the minute crustaceans known as ostracods^[7] and conchostracans.^[8]

Anatomy

Bivalves have bilaterally symmetrical and laterally flattened bodies, with a blade-shaped foot, vestigial head and no radula.^[9][10] At the dorsal or back region of the shell is the hinge point or line, which contain the umbo and beak and the lower, curved margin is the ventral or underside region. The anterior or front of the shell is where the byssus (when present) and foot are located, and the posterior of the shell is where the siphons are located. With the hinge uppermost and with the anterior edge of the animal towards the viewer's left, the valve facing the viewer is the left valve and the opposing valve the right.^[11][12] Many bivalves such as clams, which appear upright, are evolutionarily lying on their side.

Mantle and shell

The shell is composed of two calcareous valves held together by a ligament. The valves are made of either calcite, as is the case in oysters, or both calcite and aragonite. Sometimes, the aragonite forms an inner, nacreous layer, as is the case in the order Pteriida. In other taxa, alternate layers of calcite and aragonite are laid down.^[13] The ligament and byssus, if calcified, are composed of aragonite.^[13] The outermost layer of the shell is the periostracum, a thin layer composed of horny conchiolin. The periostracum is secreted by the outer mantle and is easily abraded.^[14] The outer surface of the valves is often sculpted, with clams often having concentric striations, scallops having radial ribs and oysters a latticework of irregular markings.^[15]

In all molluscs, the mantle forms a thin membrane that covers the animal's body and extends out from it in flaps or lobes. In bivalves, the mantle lobes secrete the valves, and the mantle crest secretes the whole hinge mechanism consisting of ligament, byssus threads (where present), and teeth.^[16] The posterior mantle edge may have two elongated extensions known as siphons, through one of which water is inhaled, and the other expelled.^[17] The siphons retract into a cavity, known as the pallial sinus.^[18]

The shell grows larger when more material is secreted by the mantle edge, and the valves themselves thicken as more material is secreted from the general mantle surface. Calcareous matter comes from both its diet and the surrounding seawater. Concentric rings on the exterior of a valve are commonly used to age bivalves. For some groups, a more precise method for determining the age of a shell is by cutting a cross section through it and examining the incremental growth bands.^[19]

The shipworms, in the family Teredinidae have greatly elongated bodies, but their shell valves are much reduced and restricted to the anterior end of the body, where they function as scraping organs that permit the animal to dig tunnels through wood.^[20]

Muscles and ligaments

The main muscular system in bivalves is the posterior and anterior adductor muscles. These muscles connect the two valves and contract to close the shell. The valves are also joined dorsally by the hinge ligament, which is an extension of the periostracum. The ligament is responsible for opening the shell, and works against the adductor muscles when the animal opens and closes.^[21] Retractor muscles connect the mantle to the edge of the shell, along a line known as the pallial line.^[22][16] These muscles pull the mantle though the valves.^[16]

In sedentary or recumbent bivalves that lie on one valve, such as the oysters and scallops, the anterior adductor muscle has been lost and the posterior muscle is positioned centrally.^[23] In species that can swim by flapping their valves, a single, central adductor muscle occurs. These muscles are composed of two types of muscle fibres, striated muscle bundles for fast actions and smooth muscle bundles for maintaining a steady pull.^[24] Paired pedal protractor and retractor muscles operate the animal's foot.^[11][25][26]

Nervous system

The sedentary habits of the bivalves have meant that in general the nervous system is less complex than in most other molluscs. The animals have no brain; the nervous system consists of a nerve network and a series of paired ganglia. In all but the most primitive bivalves, two cerebropleural ganglia are on either side of the oesophagus. The cerebral ganglia control the sensory organs, while the pleural ganglia supply nerves to the mantle cavity. The pedal ganglia, which control the foot, are at its base, and the visceral ganglia, which can be quite large in swimming bivalves, are under the posterior adductor muscle. These ganglia are both connected to the cerebropleural ganglia by nerve fibres. Bivalves with long siphons may also have siphonal ganglia to control them.^[27][28]

Senses

The sensory organs of bivalves are largely located on the posterior mantle margins. The organs are usually mechanoreceptors or chemoreceptors, in some cases located on short tentacles. The osphradium is a patch of sensory cells located below the posterior adductor muscle that may serve to taste the water or measure its turbidity. Statocysts within the organism help the bivalve to sense and correct its orientation.^[28] In the order Anomalodesmata, the inhalant siphon is surrounded by vibration-sensitive tentacles for detecting prey.^[29] Many bivalves have no eyes, but a few members of the Arcoidea, Limopsoidea, Mytiloidea, Anomioidea, Ostreoidea, and Limoidea have simple eyes on the margin of the mantle. These consist of a pit of photosensory cells and a lens.^[30] Scallops have more complex eyes with a lens, a two-layered retina, and a concave mirror.^[31] All bivalves have light-sensitive cells that can detect a shadow falling over the animal.^[27]

Circulation and respiration

Bivalves have an open circulatory system that bathes the organs in blood (hemolymph). The heart has three chambers: two auricles receiving blood from the gills, and a single ventricle. The ventricle is muscular and pumps hemolymph into the aorta, and then to the rest of the body. Some bivalves have a single aorta, but most also have a second, usually smaller, aorta serving the hind parts of the animal.^[32] The hemolymph usually lacks any respiratory pigment.^[33] In the carnivorous genus Poromya, the hemolymph has red amoebocytes containing a haemoglobin pigment.^[34]

The paired gills are located posteriorly and consist of hollow tube-like filaments with thin walls for gas exchange. The respiratory demands of bivalves are low, due to their relative inactivity. Some freshwater species, when exposed to the air, can gape the shell slightly and gas exchange can take place.^[35][36] Oysters, including the Pacific oyster (Magallana gigas), are recognized as having varying metabolic responses to environmental stress, with changes in respiration rate being frequently observed.^[37]

Digestive system

Modes of feeding

Most bivalves are filter feeders, using their gills to capture particulate food such as phytoplankton from the water. Protobranchs feed in a different way, scraping detritus from the seabed, and this may be the original mode of feeding used by all bivalves before the gills became adapted for filter feeding. These primitive bivalves hold on to the bottom with a pair of tentacles at the edge of the mouth, each of which has a single palp, or flap. The tentacles are covered in mucus, which traps the food, and cilia, which transport the particles back to the palps. These then sort the particles, rejecting those that are unsuitable or too large to digest, and conveying others to the mouth.^[38]

In more advanced bivalves, water is drawn into the shell from the posterior ventral surface of the animal, passes upwards through the gills, and doubles back to be expelled just above the intake. There may be two elongated, retractable siphons reaching up to the seabed, one each for the inhalant and exhalant streams of water. The gills of filter-feeding bivalves are known as ctenidia and have become highly modified to increase their ability to capture food. For example, the cilia on the gills, which originally served to remove unwanted sediment, have become adapted to capture food particles, and transport them in a steady stream of mucus to the mouth. The filaments of the gills are also much longer than those in more primitive bivalves, and are folded over to create a groove through which food can be transported. The structure of the gills varies considerably, and can serve as a useful means for classifying bivalves into groups.^[38][39]

A few bivalves, such as the granular poromya (Poromya granulata), are carnivorous, eating much larger prey than the tiny microalgae consumed by other bivalves. Muscles draw water in through the inhalant siphon which is modified into a cowl-shaped organ, sucking in prey. The siphon can be retracted quickly and inverted, bringing the prey within reach of the mouth. The gut is modified so that large food particles can be digested.^[34]

The unusual genus, Entovalva, is endosymbiotic, being found only in the oesophagus of sea cucumbers. It has mantle folds that completely surround its small valves. When the sea cucumber sucks in sediment, the bivalve allows the water to pass over its gills and extracts fine organic particles. To prevent itself from being swept away, it attaches itself with byssal threads to the host's throat. The sea cucumber is unharmed.^[40]

Digestive tract

The digestive tract of typical bivalves consists of an oesophagus, stomach, and intestine. Protobranch stomachs have a mere sac attached to them while filter-feeding bivalves have elongated rod of solidified mucus referred to as the "crystalline style" projected into the stomach from an associated sac. Cilia in the sac cause the style to rotate, winding in a stream of food-containing mucus from the mouth, and churning the stomach contents. This constant motion propels food particles into a sorting region at the rear of the stomach, which distributes smaller particles into the digestive glands, and heavier particles into the intestine.^[41] Waste material is consolidated in the rectum and voided as pellets into the exhalent water stream through an anal pore. Feeding and digestion are synchronized with diurnal and tidal cycles.^[42]

Carnivorous bivalves generally have reduced crystalline styles and the stomach has thick, muscular walls, extensive cuticular linings and diminished sorting areas and gastric chamber sections.^[43]

Excretory system

The excretory organs of bivalves are a pair of nephridia. Each of these consists of a long, looped, glandular tube, which opens into the pericardium, and a bladder to store urine. They also have pericardial glands either line the auricles of the heart or attach to the pericardium, and serve as extra filtration organs. Metabolic waste is voided from the bladders through a nephridiopore near the front of the upper part of the mantle cavity and excreted.^[44][45]

Reproduction and development

The sexes are usually separate in bivalves but some hermaphroditism is known. The gonads either open into the nephridia or through a separate pore into a chamber over the gills.^[46][47] The ripe gonads of males and females release sperm and eggs into the water column. Spawning may take place continually or be triggered by environmental factors such as day length, water temperature, or the presence of sperm in the water. Some species are "dribble spawners", releasing gametes during protracted period that can extend for weeks. Others are mass spawners and release their gametes in batches or all at once.^[48]

Fertilization is usually external. Typically, a short stage lasts a few hours or days before the eggs hatch into trochophore larvae. These later develop into veliger larvae which settle on the seabed and undergo metamorphosis into adults.^[46][49] In some species, such as those in the genus Lasaea, females draw water containing sperm in through their inhalant siphons and fertilization takes place inside the female. These species then brood the young inside their mantle cavity, eventually releasing them into the water column as veliger larvae or as crawl-away juveniles.^[50]

Most of the bivalve larvae that hatch from eggs in the water column feed on diatoms or other phytoplankton. In temperate regions, about 25% of species are lecithotrophic, depending on nutrients stored in the yolk of the egg where the main energy source is lipids. The longer the period is before the larva first feeds, the larger the egg and yolk need to be. The reproductive cost of producing these energy-rich eggs is high and they are usually smaller in number. For example, the Baltic tellin (Macoma balthica) produces few, high-energy eggs. The larvae hatching out of these rely on the energy reserves and do not feed. After about four days, they become D-stage larvae, when they first develop hinged, D-shaped valves. These larvae have a relatively small dispersal potential before settling out. The common mussel (Mytilus edulis) produces 10 times as many eggs that hatch into larvae and soon need to feed to survive and grow. They can disperse more widely as they remain planktonic for a much longer time.^[51]

Freshwater bivalves have different lifecycle. Sperm is drawn into a female's gills with the inhalant water and internal fertilization takes place. The eggs hatch into glochidia larvae that develop within the female's shell. Later they are released and attach themselves parasitically to the gills or fins of a fish host. After several weeks they drop off their host, undergo metamorphosis and develop into adults on the substrate.^[46]

Some of the species in the freshwater mussel family, Unionidae, commonly known as pocketbook mussels, have evolved an unusual reproductive strategy. The female's mantle protrudes from the shell and develops into an imitation small fish, complete with fish-like markings and false eyes. This decoy moves in the current and attracts the attention of real fish. Some fish see the decoy as prey, while others see a conspecific. They approach for a closer look and the mussel releases huge numbers of larvae from its gills, dousing the inquisitive fish with its tiny, parasitic young. These glochidia larvae are drawn into the fish's gills, where they attach and trigger a tissue response that forms a small cyst around each larva. The larvae then feed by breaking down and digesting the tissue of the fish within the cysts. After a few weeks they release themselves from the cysts and fall to the stream bed as juvenile molluscs.^[52]

Comparison with brachiopods

Brachiopods are shelled marine organisms that superficially resemble bivalves in that they are of similar size and have a hinged shell in two parts. However, brachiopods evolved from a very different ancestral line, and the resemblance to bivalves only arose because they occupy similar ecological niches. The differences between the two groups are due to their separate ancestral origins. Different initial structures have been adapted to solve the same problems, a case of convergent evolution. In modern times, brachiopods are not as common as bivalves.^[53]

Both groups have a shell consisting of two valves, but the organization of the shell is quite different in the two groups. In brachiopods, the two valves are positioned on the dorsal and ventral surfaces of the body, while in bivalves, the valves are on the left and right sides of the body, and are, in most cases, mirror images of one other. Brachiopods have a lophophore, a coiled, rigid cartilaginous internal apparatus adapted for filter feeding, a feature shared with two other major groups of marine invertebrates, the bryozoans and the phoronids. Some brachiopod shells are made of calcium phosphate but most are calcium carbonate in the form of the biomineral calcite, whereas bivalve shells are always composed entirely of calcium carbonate, often in the form of the biomineral aragonite.^[54]

Evolutionary history

The Cambrian explosion took place around 540 to 520 million years ago (Mya). In this geologically brief period, all the major animal phyla diverged and these included the first creatures with mineralized skeletons. Brachiopods and bivalves made their appearance at this time, and left their fossilized remains behind in the rocks.^[55]

Possible early bivalves include Pojetaia and Fordilla; these probably lie in the stem rather than crown group. Watsonella and Anabarella are perceived to be (earlier) close relatives of these taxa.^[56] Only five genera of supposed Cambrian "bivalves" exist, the others being Tuarangia, Camya and Arhouriella and potentially Buluniella.^[57]

Bivalve fossils can be formed when the sediment in which the shells are buried hardens into rock. Often, the impression made by the valves remains as the fossil rather than the valves. During the Early Ordovician, a great increase in the diversity of bivalve species occurred, and the dysodont, heterodont, and taxodont dentitions evolved. By the Early Silurian, the gills were becoming adapted for filter feeding, and during the Devonian and Carboniferous periods, siphons first appeared, which, with the newly developed muscular foot, allowed the animals to bury themselves deep in the sediment.^[58]

By the middle of the Paleozoic, around 400 Mya, the brachiopods were among the most abundant filter feeders in the ocean, and over 12,000 fossil species are recognized.^[59] By the Permian–Triassic extinction event 250 Mya, bivalves were undergoing a huge radiation of diversity. The bivalves were hard hit by this event, but re-established themselves and thrived during the Triassic period that followed. In contrast, the brachiopods lost 95% of their species diversity.^[54] The ability of some bivalves to burrow and thus avoid predators may have been a major factor in their success. Other new adaptations within various families allowed species to occupy previously unused evolutionary niches. These included increasing relative buoyancy in soft sediments by developing spines on the shell, gaining the ability to swim, and in a few cases, adopting predatory habits.^[58]

For a long time, bivalves were thought to be better adapted to aquatic life than brachiopods were, outcompeting and relegating them to minor niches in later ages. These two taxa appeared in textbooks as an example of replacement by competition. Evidence given for this included the fact that bivalves needed less food to subsist because of their energetically efficient ligament-muscle system for opening and closing valves. All this has been broadly disproven, though; rather, the prominence of modern bivalves over brachiopods seems due to chance disparities in their response to extinction events.^[60]

Diversity of extant bivalves

The adult maximum size of living species of bivalve ranges from 0.52 mm (0.02 in) in Condylonucula maya,^[61] a nut clam, to a length of 1,532 millimetres (60.3 in) in Kuphus polythalamia, an elongated, burrowing shipworm.^[62] However, the species generally regarded as the largest living bivalve is the giant clam Tridacna gigas, which can grow to a length of 1,200 mm (47 in) and a weight of more than 200 kg (441 lb).^[63] The largest known extinct bivalve is a species of Platyceramus whose fossils measure up to 3,000 mm (118 in) in length.^[64]

In his 2010 treatise, Compendium of Bivalves, Markus Huber gives the total number of living bivalve species as about 9,200 combined in 106 families.^[65] Huber states that the number of 20,000 living species, often encountered in literature, could not be verified and presents the following table to illustrate the known diversity: