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CHAPTER 16 Molluscs Phylum Mollusca

Fluted giant clam, Tridacna squamosa.

A Significant Space space within the mesoderm, the coelom. This meant that the Long ago in the Precambrian era, the most complex animals space was lined with mesoderm and the organs were sus- populating the seas were acoelomate. They must have been pended by mesodermal membranes, the mesenteries. Not inefficient burrowers, and they were unable to exploit the only could the coelom serve as an efficient hydrostatic rich subsurface ooze. Any that developed fluid-filled spaces skeleton, with circular and longitudinal body-wall muscles within the body would have had a substantial selective acting as antagonists, but a more stable arrangement of advantage because these spaces could serve as a hydro- organs with less crowding resulted. Mesenteries provided an static skeleton and improve burrowing efficiency. ideal location for networks of blood vessels, and the ali- The simplest, and probably the first, mode of achieving mentary canal could become more muscular, more highly a fluid-filled space within the body was retention of the specialized, and more diversified without interfering with embryonic blastocoel, as in pseudocoelomates. This was not other organs. the best evolutionary solution because, for example, the Development of a coelom was a major step in the evo- organs lay loose in the body cavity. lution of larger and more complex forms. All the major Some descendants of Precambrian acoelomate organ- groups in chapters to follow are coelomates. isms evolved a more elegant arrangement: a fluid-filled

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326 PART 3 The Diversity of Animal Life

Position in Animal common ancestor with annelids 3. The efficiency of the respiratory Kingdom before the advent of metamerism. and circulatory systems in the 5. All organ systems are present and cephalopods has made greater body 1. Molluscs are one of the major groups well developed. size possible. Invertebrates reach their of true coelomate animals. largest size in some cephalopods. 2. They belong to the protostome Biological Contributions 4. They have a fleshy mantle that in branch, or schizocoelous coelomates, most cases secretes a shell and is and have spiral cleavage and 1. In molluscs gaseous exchange occurs variously modified for a number of determinate (mosaic) development. not only through the body surface as functions. 3. Many molluscs have a trochophore in phyla discussed previously, but 5. Features unique to the phylum are the larva similar to trochophore larvae of also in specialized respiratory radula and the muscular foot. marine annelids and other marine organs in the form of gills or lungs. 6. The highly developed direct eye of protostomes. Developmental evidence 2. Most classes have an open cephalopods is similar to the indirect thus indicates that molluscs and circulatory system with pumping eye of vertebrates but arises as a skin annelids share a common ancestor. heart, vessels, and blood sinuses. In derivative in contrast to the brain eye 4. Because molluscs are not metameric, most cephalopods the circulatory of vertebrates. they must have diverged from their system is closed.

The Molluscs Mollusca (mol-luska) (L. molluscus, soft) is one of the largest animal phyla after Arthropoda. There are nearly 50,000 living species and some 35,000 fossil species. The name Mollusca indicates one of their distinctive char- acteristics, a soft body. This very diverse group (Figure 16-1) includes chitons, tooth shells, snails, slugs, A D nudibranchs, sea butterflies, clams, mussels, oysters, squids, octopuses, and nautiluses. The group ranges from fairly simple organisms to some of the most complex of invertebrates, and in size from almost microscopic to the giant squid Architeuthis. These huge molluscs may grow to 18 m long, including their tentacles. They may weigh 450 kg (1,000 pounds). The shells of some giant clams, Tridacna gigas, which inhabit Indo-Pacific coral B E reefs, reach 1.5 m in length and weigh more than 225 kg. These are extremes, Figure 16-1 however, for probably 80% of all mol- Molluscs: a diversity of life forms. The basic luscs are less than 5 cm in maximum body plan of this ancient group has become shell size. The phylum includes some variously adapted for different habitats. A, A of the most sluggish and some of the chiton (Tonicella lineata), Class Polyplacophora. B, A marine snail (Calliostoma annulata), Class swiftest and most active invertebrates. Gastropoda. C, A nudibranch (Chromodoris sp.) It includes herbivorous grazers, preda- Class Gastropoda. D, Pacific giant clam ceous carnivores, filter feeders, detritus (Panope abrupta), with siphons to the left, Class feeders, and parasites. Bivalvia. E, An octopus (Octopus briareus), Molluscs are found in a great range Class Cephalopoda, forages at night on a Caribbean coral reef. of habitats, from the tropics to polar C hic09617_ch16.qxd 5/30/00 12:45 PM Page 327

CHAPTER 16 Molluscs 327

seas, at altitudes exceeding 7000 m, in ponds, lakes, and streams, on mud Characteristics of Phylum (usually three chambered), blood flats, in pounding surf, and in open Mollusca vessels, and sinuses; respiratory pig- ocean from the surface to abyssal ments in blood 1. Body bilaterally symmetrical (bilater- depths. Most of them live in the sea, 8. Gaseous exchange by gills, lungs, al asymmetry in some); unsegment- and they represent a variety of life- mantle, or body surface ed; often with definite head styles, including bottom feeders, bur- 9. One or two kidneys (metaneph- 2. Ventral body wall specialized as a rowers, borers, and pelagic forms. ridia) opening into the pericardial muscular foot, variously modified cavity and usually emptying into the According to fossil evidence, mol- but used chiefly for locomotion luscs originated in the sea, and most of mantle cavity 3. Dorsal body wall forms pair of folds 10. Nervous system of paired cerebral, them have remained there. Much of called the mantle, which encloses their evolution occurred along the pleural, pedal, and visceral ganglia, the mantle cavity, is modified into with nerve cords and subepidermal shores, where food was abundant and gills or lungs, and secretes the plexus; ganglia centralized in nerve habitats were varied. Only bivalves shell (shell absent in some) ring in gastropods and cephalopods and gastropods moved into brackish 4. Surface epithelium usually ciliated 11. Sensory organs of touch, smell, taste, and freshwater habitats. As filter feed- and bearing mucous glands and sen- equilibrium, and vision (in some); ers, bivalves were unable to leave sory nerve endings eyes highly developed in aquatic surroundings. Only snails (gas- 5. Coelom limited mainly to area cephalopods tropods) actually invaded the land. around heart, and perhaps lumen of 12. Internal and external ciliary tracts Terrestrial snails are limited in their gonads and part of kidneys often of great functional importance range by their need for humidity, shel- 6. Complex digestive system; rasping 13. Both monoecious and dioecious ter, and presence of calcium in the soil. organ (radula) usually present; anus forms; spiral cleaveage; larva primi- Many kinds of molluscs are used usually emptying into mantle cavity tively a trochophore, many with a as food. Pearl buttons are obtained 7. Open circulatory system (mostly veliger larva, some with direct from shells of bivalves. The Mississippi closed in cephalopods) of heart development and Missouri river basins have fur- nished material for most of this indus- try in the United States; however, supplies are becoming so depleted that attempts are being made to propagate bers of class Polyplacophora (chitons) Form and Function bivalves artificially. Pearls, both natural are common to abundant marine ani- and cultured, are produced in the mals, especially in the intertidal zone. The enormous variety, great beauty, shells of clams and oysters, most of Bivalves (class Bivalvia) have evolved and easy availability of shells of mol- them in a marine oyster, Meleagrina, many species, both marine and fresh- luscs have made shell collecting a pop- found around eastern Asia. water. Largest and most intelligent of ular pastime. However, many amateur Some molluscs are destructive. Bur- all invertebrates are in the class shell collectors, even though able to rowing shipworms, which are bivalves Cephalopoda (squids, octopuses, and name hundreds of the shells that grace of several species (see Figure 16-27), others). Most abundant and wide- our beaches, know very little about the do great damage to wooden ships and spread of molluscs, however, are snails living animals that created those shells wharves. To prevent the ravages of and their relatives (class Gastropoda). and once lived in them. Reduced to its shipworms, wharves must be either Although enormously diverse, mol- simplest dimensions, the mollusc body creosoted or built of concrete (unfortu- luscs have in common a basic body plan may be said to consist of a head- nately, some ignore the creosote, and plan, which is described later in the foot portion and a visceral mass por- some bivalves bore into concrete). chapter. It seems peculiar, though, that tion (Figure 16-2). The head-foot is the Snails and slugs frequently damage molluscs have failed to exploit the more active area, containing the feed- garden and other vegetation. In addi- coelom. The coelom in molluscs is lim- ing, cephalic sensory, and locomotor tion, snails often serve as intermediate ited to a space around the heart, and organs. It depends primarily on mus- hosts for serious parasites. The boring perhaps around the gonads and part of cular action for its function. The vis- snail Urosalpinx rivals sea stars in the kidneys. Although it develops ceral mass is the portion containing destroying oysters. embryonically in a manner similar to digestive, circulatory, respiratory, and In this chapter we explore the the coelom of annelids, the functional reproductive organs, and it depends various major groups of molluscs, consequences of the space are quite primarily on ciliary tracts for its func- including those that apparently met different. Some zoologists believe that tioning. Two folds of skin, outgrowths with little evolutionary success (classes molluscs arose from a flatworm-type of the dorsal body wall, make up a Caudofoveata, Solenogastres, Mono- ancestor separately from annelids and protective mantle, or pallium, which placophora, and Scaphopoda). 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328 PART 3 The Diversity of Animal Life

Intestine Heart Head-Foot Gonad Coelom Most molluscs have well-developed Stomach Nephridium heads, which bear their mouth and Digestive Shell some specialized sensory organs. Pho- gland tosensory receptors range from fairly Gill simple ones to the complex eyes of Mantle Mantle cavity cephalopods. Tentacles are often pres- ent. Within the mouth is a structure unique to molluscs, the radula, and Radula Anus usually posterior to the mouth is the chief locomotor organ, or foot.

Mouth Nerve collar Foot Retractor muscles Radula Figure 16-2 Generalized mollusc. Although this construct is often presented as a “hypothetical ancestral mollusc The radula is a rasping, protrusible, (HAM),” most experts now reject this interpretation. For example, the molluscan ancestor probably tonguelike organ found in all mol- was covered with calcareous spicules, rather than a univalve shell. Such a diagram is useful, however, luscs except bivalves and most to facilitate description of the general body plan of molluscs. solenogasters. It is a ribbonlike mem- brane on which are mounted rows of Radula tiny teeth that point backward (Fig- teeth ure 16-3). Complex muscles move the radula and its supporting cartilages (odontophore) in and out while the Odontophore membrane is partly rotated over the tips of the cartilages. There may be a few or as many as 250,000 teeth, which, when protruded, can scrape, pierce, tear, or cut. The usual function of the radula is twofold: to rasp off fine particles of food material from hard surfaces and to serve as a conveyor Esophagus belt for carrying particles in a continu- Radula ous stream toward the digestive tract. sac Odontophore As the radula wears away anteriorly, B new rows of teeth are continuously Figure 16-3 replaced by secretion at its posterior A, Diagrammatic longitudinal section of a end. The pattern and number of teeth gastropod head showing a radula and radula in a row are specific for each species sac. The radula moves back and forth over the odontophore cartilage. As the animal grazes, and are used in the classification of the mouth opens, the odontophore is thrust molluscs. Very interesting radular spe- Radula Mouth forward, the radula gives a strong scrape cializations, such as for boring through retractor backward bringing food into the pharynx, and hard materials or for harpooning prey, Odontophore the mouth closes. The sequence is repeated are found in some forms. retractor Radula rhythmically. As the radula ribbon wears out Radula anteriorly, it is continually replaced posteriorly. protractor Odontophore B, Radula of a snail prepared for microscopic Foot A protractors examination. The molluscan foot (see Figure 16-2) may be variously adapted for locomo- tion, for attachment to a substratum, or and body wall called the mantle cav- mass produce the great diversity of for a combination of functions. It is ity (pallial cavity). The mantle cavity patterns observed in Mollusca. Greater usually a ventral, solelike structure in houses gills (ctenidia) or a lung, and emphasis on either the head-foot por- which waves of muscular contraction in some molluscs the mantle secretes a tion or the visceral mass portion can be effect a creeping locomotion. How- protective shell over the visceral mass. observed in various classes of mol- ever, there are many modifications, Modifications of the structures that luscs. such as the attachment disc of limpets, make up the head-foot and the visceral the laterally compressed “hatchet foot” hic09617_ch16.qxd 5/30/00 12:46 PM Page 329

CHAPTER 16 Molluscs 329

Shell

H2O Shell Mantle

H2O Axis Periostracum

Prismatic Filament layer

Nacre

Mantle Pearl Mantle Attaching Outer folds membrane mantle epithelium New Skeletal AB rod periostracum

Figure 16-4 Figure 16-5 Primitive condition of mollusc ctenidium. A, Diagrammatic vertical section of shell and mantle of a bivalve. The outer mantle epithelium secretes Circulation of water between gill filaments is by the shell; the inner epithelium is usually ciliated. B, Formation of pearl between mantle and shell as a cilia, and blood diffuses through the filament parasite or bit of sand under the mantle becomes covered with nacre. from the afferent vessel to the efferent vessel. Black arrows are ciliary cleansing currents.

of bivalves, or the siphon for jet mollusc. It usually houses respiratory fuses from an afferent vessel in the propulsion in squids and octopuses. organs (gills or lung), which develop central axis through the filament to an Secreted mucus is often used as an aid from the mantle, and the mantle’s own efferent vessel. Direction of blood to adhesion or as a slime tract by small exposed surface serves also for movement is opposite to the direction molluscs that glide on cilia. gaseous exchange. Products from the of water movement, thus establishing a In snails and bivalves the foot is digestive, excretory, and reproductive countercurrent exchange mechanism extended from the body hydraulically, systems are emptied into the mantle (see p. 527). The two ctenidia are by engorgement with blood. Bur- cavity. In aquatic molluscs a continu- located on opposite sides of the mantle rowing forms can extend the foot into ous current of water, kept moving by cavity and are arranged so that the the mud or sand, enlarge it with surface cilia or by muscular pumping, cavity is functionally divided into an blood pressure, then use the engorged brings in oxygen and, in some forms, incurrent chamber and an excurrent foot as an anchor to draw the body food; flushes out wastes; and carries chamber. Such gills are found in less forward. In pelagic (free-swimming) reproductive products out to the envi- derived gastropods, but they are vari- forms the foot may be modified into ronment. In aquatic forms the mantle ously modified in many molluscs. winglike parapodia, or thin, mobile fins is usually equipped with sensory for swimming. receptors for sampling environmental water. In cephalopods (squids and Shell Visceral Mass octopuses) the muscular mantle and its The shell of a mollusc, when present, cavity create jet propulsion used in is secreted by the mantle and is lined Mantle and Mantle Cavity locomotion. Many molluscs can with- by it. Typically there are three layers The mantle is a sheath of skin, extend- draw their head or foot into the mantle (Figure 16-5A). The periostracum is ing from the visceral mass, that hangs cavity, which is surrounded by the the outer horny layer, composed of an down on each side of the body, pro- shell, for protection. organic substance called conchiolin, tecting the soft parts and creating In primitive form, a mollusc cteni- which consists of quinone-tanned pro- between itself and the visceral mass a dium (gill) consists of a long, flattened tein. It helps to protect underlying cal- space called the mantle cavity. The axis extending from the wall of the careous layers from erosion by boring outer surface of the mantle secretes the mantle cavity (Figure 16-4). Many leaf- organisms. It is secreted by a fold of shell. like gill filaments project from the the mantle edge, and growth occurs The mantle cavity (Figure 16-2) central axis. Water is propelled by cilia only at the margin of the shell. On the plays an enormous role in the life of a between gill filaments, and blood dif- older parts of the shell the periostracum hic09617_ch16.qxd 6/19/00 10:17 AM Page 330

330 PART 3 The Diversity of Animal Life

Apical tuft of cilia

Mouth Band of cilia (prototroch) Mesoderm Figure 16-7 Anus Veliger of a snail, Pedicularia, swimming. The adults are parasitic on corals. The ciliated process Figure 16-6 (velum) develops from the prototroch of the trochophore (Figure 16-6). Generalized trochophore larva. Molluscs and annelids with primitive embryonic development Internal Structure and Function egg in many molluscs is a trocho- have trochophore larvae, as do several other phyla. Gaseous exchange occurs through the phore, which is also the ancestral lar- body surface, particularly the mantle, val type of the annelids (Figure 16-6). and in specialized respiratory organs Direct metamorphosis of the trocho- such as ctenidia, secondary gills, and phore into a small juvenile, as in often becomes worn away. The middle lungs. There is an open circulatory chitons, is viewed as ancestral for prismatic layer is composed of system with a pumping heart, blood molluscs, and the intervention of densely packed prisms of calcium car- vessels, and blood sinuses. Most another free-swimming larval stage, a bonate laid down in a protein matrix. It cephalopods have a closed blood sys- veliger, as in many gastropods and is secreted by the glandular margin of tem with heart, vessels, and capillaries. bivalves, is a derived character. The the mantle, and increase in shell size The digestive tract is complex and veliger (Figure 16-7) has the begin- occurs at the shell margin as the ani- highly specialized, according to feed- nings of a foot, shell, and mantle. In mal grows. The inner nacreous layer ing habits of the various molluscs, and many molluscs the trochophore stage of the shell lies next to the mantle and is usually provided with extensive cil- occurs in the egg, and a veliger hatches is secreted continuously by the mantle iary tracts. Most molluscs have a pair of to become the only free-swimming surface, so that it increases in thickness kidneys (metanephridia, a type of stage. Cephalopods, freshwater and during the life of the animal. The cal- nephridium in which the inner end some marine snails, and some fresh- careous nacre is laid down in thin lay- opens into the coelom by a nephro- water bivalves have no free-swimming ers. Very thin and wavy layers produce stome); ducts of the kidneys in many larvae, and juveniles hatch directly the iridescent mother-of-pearl found in forms also serve for discharge of eggs from eggs. abalones (Haliotis), chambered nau- and sperm. tiluses (Nautilus), and many bivalves. The nervous system consists of Such shells may have 450 to 5000 fine several pairs of ganglia with connecting parallel layers of crystalline calcium Trochophore larvae (Figure 16-6) are nerve cords, and it is generally simpler minute, translucent, and more or less pear carbonate (aragonite) for each cen- than that of annelids and arthropods. shaped and have a prominent circlet of cilia timeter of thickness. The nervous system contains neurose- (prototroch) and sometimes one or two Freshwater molluscs usually have cretory cells that, at least in certain accessory circlets.They are found in a thick periostracum that gives some airbreathing snails, produce a growth molluscs and annelids with primitive protection against acids produced in hormone and function in osmoregula- embryonic development and are consid- the water by decay of leaf litter. In tion. There are various types of highly ered one of the evidences for common many marine molluscs the perios- specialized sense organs. phylogenetic origin of the two phyla. Some tracum is relatively thin, and in some it form of trochophore-like larva is also found in marine turbellarians, nemertines, bra- is absent. There is great variation in Reproduction and shell structure. Calcium for the shell chiopods, phoronids, sipunculids, and echi- comes from environmental water or Life History urids, and it probably reflects some phylogenetic relationship among all these soil or from food. The first shell Most molluscs are dioecious, although phyla. Some zoologists unite them in a appears during the larval period and some are hermaphroditic. The free- taxon called Trochozoa. grows continuously throughout life. swimming larva that emerges from the hic09617_ch16.qxd 6/14/00 10:41 PM Page 331

CHAPTER 16 Molluscs 331 Classes of Molluscs spicules in their integument, with reduced head, and without nephridia. For more than 50 years five classes of Solenogasters, however, usually have living molluscs were recognized: Am- no radula and no gills (although sec- phineura, Gastropoda, Scaphopoda, ondary respiratory structures may be Bivalvia (also called Pelecypoda), and present). Their foot is represented by a Cephalopoda. Discovery of Neopilina midventral, narrow furrow, the pedal in the 1950s added another class groove. They are hermaphroditic. (Monoplacophora), and Hyman* con- Rather than burrowing, solenogasters tended that solenogasters and chitons live free on the bottom, and they make up separate classes (Polypla- often live and feed on cnidarians. cophora and Aplacophora), lapsing the Solenogasters are also a small group, name Amphineura. Recognition of numbering about 250 species. important differences between organ- isms such as Chaetoderma and other solenogasters has separated Apla- Class Monoplacophora cophora into the sister groups Caudo- Until 1952 it was thought that Mono- foveata and Solenogastres.† placophora were extinct; they were known only from Paleozoic shells. Class Caudofoveata However, in that year living specimens of Neopilina (Gr. neo, new, pilos, Members of class Caudofoveata are felt cap) were dredged up from the wormlike, marine organisms ranging ocean bottom near the west coast of from 2 to 140 mm in length (see Fig- Costa Rica. Nearly a dozen species of ure 16-41). They are mostly burrowers monoplacophorans are now known. and orient themselves vertically, with These molluscs are small and have a the terminal mantle cavity and gills at low, rounded shell and a creeping foot Figure 16-8 the entrance of the burrow. They feed (Figure 16-8). They have superficial Neopilina, class Monoplacophora. Living on microorganisms and detritus. They resemblance to limpets, but unlike specimens range from 3 mm to about 3 cm in have no shell, but their bodies are cov- most other molluscs, a number of length. A, Ventral view. B, Dorsal view. ered with calcareous scales. There are organs are serially repeated. Such se- no spicules or scales on the oral pedal rial repetition occurs to a more limited shield, an organ apparently associated extent in chitons. Neopilina has five which have the form of eyes in some with food selection and intake. A rad- pairs of gills, two pairs of auricles, six chitons, pierce the plates. ula is present, although reduced in pairs of nephridia, one or two pairs of Most chitons are small (2 to 5 cm); some, and sexes are separate. This lit- gonads, and a ladderlike nervous sys- the largest, Cryptochiton (Gr. crypto, tle group has fewer than 70 species; tem with 10 pairs of pedal nerves. The hidden, chiton, coat of mail), rarely however, its features may be closer to mouth bears the characteristic radula. exceeds 30 cm. They prefer rocky sur- those of the common ancestor of mol- faces in intertidal regions, although luscs than any other living molluscs. some live at great depths. Most chitons Class Polyplacophora: are stay-at-home organisms, straying only very short distances for feeding. Class Solenogastres Chitons In feeding, the radula projects from the Solenogasters (see Figure 16-41) and Chitons (Gr. coat of mail, tunic) (Fig- mouth to scrape algae from the rocks. caudofoveates were formerly united ures 16-9 and 16-10) represent a some- The radula is reinforced with the iron- in class Aplacophora, and some zo- what more diverse molluscan group. containing mineral, magnetite. A chi- ologists retain the name Aplacophora They are rather flattened dorsoven- ton clings tenaciously to its rock with for solenogasters, excluding caudo- trally and have a convex dorsal surface its broad, flat foot. If detached, it can foveates. Both caudofoveates and that bears eight articulating limy plates, roll up like an armadillo for protection. solenogasters are marine, wormlike, or valves, hence their name Poly- The mantle forms a girdle around shell-less, with calcareous scales or placophora (“many plate bearers”). the margin of the plates, and in some The plates overlap posteriorly and are species mantle folds cover part or all of * Hyman, L. H. 1967. The invertebrates, vol. VI. New usually dull colored to match the rocks the plates. Compared with the primi- York, McGraw-Hill Book Company. to which chitons cling. Their head and tive condition, the mantle cavity has † Boss, K. J. 1982. Mollusca. In Parker, S. P. ed., Syn- opsis and classification of living organisms, vol. 1. New cephalic sensory organs are reduced, been extended along the side of the York, McGraw-Hill Book Company. but photosensitive structures (esthetes), foot, and the gills have been increased hic09617_ch16.qxd 5/30/00 12:48 PM Page 332

332 PART 3 The Diversity of Animal Life

Intestine Aorta A Gonad Plate B Radula Heart

Nerve Pericardium Ventral ring nerves Mantle Foot Kidney Pallial groove girdle with gills

Digestive Gonopore Nephridiopore Nephrostome Gonad Mouth gland Stomach Kidney Anus Foot Anus C Nerve cords Intestine

Mouth Nephrostome (opening into pericardium) NephridioporeGonopore Figure 16-9 Anatomy of a chiton (class Polyplacophora). A, Longitudinal section. B, Transverse section. C, External ventral view.

posteriorly, bringing a continuous sup- can body plan has taken a new direc- ply of oxygen to the gills. At low tide tion, with the mantle wrapped around the margins of the mantle can be the viscera and fused to form a tube. tightly pressed to the substratum to Most scaphopods are 2.5 to 5 cm long, diminish water loss, but in some cir- although they range from 4 mm to cumstances, the mantle margins can be 25 cm long. Dentalium (L. dentis, tooth) held open for limited air breathing. A is a common Atlantic genus. pair of osphradia (sense organs for The foot, which protrudes through sampling water) are found in the man- the larger end of the shell, is used to tle grooves near the anus of many burrow into mud or sand, always leav- chitons. ing the small end of the shell exposed to Blood pumped by the three- the water above (Figure 16-11). Respi- chambered heart reaches the gills by ratory water circulates through the way of an aorta and sinuses. A pair of mantle cavity both by movements of the kidneys (metanephridia) carries waste foot and ciliary action (Figure 16-11). from the pericardial cavity to the exte- Gaseous exchange occurs in the man- rior. Two pairs of longitudinal nerve tle, for gills are absent. Most food is cords are connected in the buccal detritus and protozoa from the substra- region. tum. It is caught on cilia of the foot or Figure 16-10 Sexes are separate in most chitons, on the mucus-covered, ciliated knobs Mossy chiton, Mopalia muscosa. The upper and trochophore larvae metamorphose of the long tentacles extending from surface of the mantle, or “girdle,” is covered with hairs and bristles, an adaptation for defense. directly into juveniles, without an inter- the head (captacula) and is conveyed vening veliger stage. to the nearby mouth. A radula carries food to a crushing gizzard. The captac- ula may serve some sensory function, in number. Thus the gills are sus- Class Scaphopoda but eyes, tentacles, and osphradia typi- pended from the roof of the mantle cal of many other molluscs are lacking. cavity along each side of the broad Scaphopoda, commonly called tusk Sexes are separate, and the larva is ventral foot. With the foot and the shells or tooth shells, are benthic a trochophore. mantle margin adhering tightly to the marine molluscs found from the subti- substrate, these grooves become dal zone to over 6000 m depth. They closed chambers, open only at the have a slender body covered with a Class Gastropoda ends. Water enters the grooves anteri- mantle and a tubular shell open at Among molluscs class Gastropoda is orly, flows across the gills, and leaves both ends. In scaphopods the mollus- by far the largest and most diverse, hic09617_ch16.qxd 5/30/00 12:49 PM Page 333

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B Apex Shell Spire

Gonad Mantle Water Whorl A Digestive Sand gland Body whorl Kidney Aperture

Stomach Inner lip Visceral Anus Outer lip ganglion Siphonal Cerebral canal ganglion Radula

Mouth Columella Pedal ganglion Foot

B A Captacula Figure 16-11 The tusk shell, Dentalium (class Scaphopoda). A, It burrows into soft mud or sand and feeds by means of its prehensile tentacles. Respiratory currents of water are drawn in by ciliary action through Busycon carica the small open end of the shell, then expelled through the same opening by muscular action. (knobbed whelk) B, Internal anatomy of Dentalium.

containing about 40,000 living and Gastropods range from micro- 15,000 fossil species. It contains so scopic forms to giant marine forms much diversity that there is no single such as Pleuroploca gigantea, a snail general term in our language that with a shell up to 60 cm long, and sea can apply to them as a whole. hares Aplysia (see Figure 16-21), They include snails, limpets, slugs, some species of which reach 1 m in whelks, conchs, periwinkles, sea length. Most of them, however, are slugs, sea hares, and sea butterflies. between 1 and 8 cm in length. Some They range from marine molluscs fossil gastropods are as much as 2 m C with many primitive characters to long. highly evolved terrestrial, air-breath- The range of gastropod habitats is ing snails and slugs. These animals large. In the sea gastropods are com- Busycon contrarium are basically bilaterally symmetrical, mon both in littoral zones and at great (lightning whelk) but because of torsion, a twisting depths, and some are even pelagic. process that occurs in the veliger Some are adapted to brackish water Figure 16-12 Shell of the whelk Busycon. A B, Busycon stage, their visceral mass has become and others to fresh water. On land they and carica, a dextral, or right-handed, shell. A asymmetrical. are restricted by such factors as min- dextral shell has the aperture on the right side The shell, when present, is always eral content of the soil and extremes when the shell is held with the apex up and the of one piece (univalve) and may be of temperature, dryness, and acidity. aperture facing the observer. C, B. contrarium, a coiled or uncoiled. Starting at the Even so, they are widespread, and sinistral, or left-handed, shell. apex, which contains the oldest and some have been found at great alti- smallest whorl, the whorls become tudes and some even in polar regions. Gastropods are usually sluggish, successively larger and spiral around Snails occupy all kinds of habitats: in sedentary animals because most of the central axis, or columella (Fig- small pools or large bodies of water, in them have heavy shells and slow loco- ure 16-12). The shell may be right woodlands, in pastures, under rocks, motion. Some are specialized for handed (dextral) or left handed in mosses, on cliffs, in trees, under- climbing, swimming, or burrowing. (sinistral), depending on the direc- ground, and on the bodies of other Shells are their chief defense, although tion of coiling. Dextral shells are far animals. They have successfully under- they are also protected by coloration more common. Direction of coiling is taken every mode of life except aerial and by secretive habits. Many snails genetically controlled. locomotion. have an operculum, a horny plate hic09617_ch16.qxd 6/14/00 10:54 PM Page 334

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that covers the shell aperture when the body is withdrawn into the shell. Others lack shells altogether. Some are distasteful to other animals, and a few such as Strombus can deal an active blow with the foot, which bears a sharp operculum. Nevertheless, they are eaten by birds, beetles, small mam- mals, fish, and other predators. Serving as intermediate hosts for many kinds of parasites, especially trematodes, snails are often harmed by larval stages of parasites.

Torsion Of all molluscs, only gastropods under- A B C go torsion. Torsion is a peculiar phe- Figure 16-13 nomenon that moves the mantle Torsion in gastropods. A, Ancestral condition before torsion. B, Hypothetical intermediate condition. C, cavity, which was originally (primi- Early gastropod, torsion complete; direction of crawling now tends to carry waste products back into mantle cavity, resulting in fouling. tively) posterior, to the front of the body, thus twisting the visceral organs as well through a 90- to 180-degree itation problem by creating the possibil- A rotation. It occurs during the veliger ity of wastes being washed back over stage, and in some species the first part the gills (fouling) and causes us to may take only a few minutes. The sec- wonder what strong evolutionary pres- ond 90 degrees typically takes a longer sures selected for such a strange realign- period. Before torsion occurs, the ment of body structures. Several expla- embryo’s mouth is anterior and the nations have been proposed, none anus and mantle cavity are posterior entirely satisfying. For example, sense B (Figure 16-13). The change is brought organs of the mantle cavity (osphradia) about by an uneven growth of the would better sample water when turned right and left muscles that attach the in the direction of travel. Certainly the shell to the head-foot. consequences of torsion and the result- After torsion, the anus and mantle ing need to avoid fouling have been cavity become anterior and open very important in the subsequent evolu- above the mouth and head. The left tion of gastropods. These consequences C gill, kidney, and heart auricle are now cannot be explored, however, until D on the right side, whereas the original another unusual fea-ture of gas- right gill, kidney, and heart auricle are tropods—coiling—has been described. now on the left, and the nerve cords have been twisted into a figure eight. Because of the space available in the Coiling mantle cavity, the animal’s sensitive Coiling, or spiral winding, of the shell head end can now be withdrawn into and visceral mass is not the same as Figure 16-14 the protection of the shell, with the torsion. Coiling may occur in the larval Evolution of shell in gastropods. A, Earliest tougher foot forming a barrier to the stage at the same time as torsion, but coiled shells were planospiral, each whorl lying outside. the fossil record shows that coiling was completely outside the preceding whorl. Varying degrees of detorsion are a separate evolutionary event and B, Better compactness was achieved by snails seen in opisthobranchs and pul- originated in gastropods earlier than in which each whorl lay partially to the side of C D, monates, and the anus opens to the torsion did. Nevertheless, all living gas- the preceding whorl. and Better weight distribution resulted when shell was moved right side or even to the posterior. tropods have descended from coiled, upward and posteriorly. However, both of these groups were torted ancestors, whether or not they derived from torted ancestors. now show these characteristics. The curious arrangement that Early gastropods had a bilaterally results from torsion poses a serious san- symmetrical planospiral shell; that is, hic09617_ch16.qxd 6/19/00 10:33 AM Page 335

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all the whorls lay in a single plane (Figure 16-14A). Such a shell was not very compact, since each whorl had to lie completely outside the preceding one. Curiously, a few modern species have secondarily returned to the pla- nospiral form. The compactness prob- lem of a planospiral shell was solved by the conispiral shape, in which each succeeding whorl is at the side of the preceding one (Figure 16-14B). However, this shape was clearly unbal- anced, hanging as it was with much weight over to one side. Better weight distribution was achieved by shifting A B the shell upward and posteriorly, with Figure 16-15 the shell axis oblique to the longitu- A, Red abalone, Haliotus rufescens. This huge, limpetlike snail is prized as food and extensively dinal axis of the foot (Figure 16-14C). marketed. Abalones are strict vegetarians, feeding especially on sea lettuce and kelp. B, Moon snail, The weight and bulk of the main Polinices lewisii. A common inhabitant of West Coast sand flats, the moon snail is a predator of clams body whorl, the largest whorl of the and mussels. It uses its radula to drill neat holes through its victim’s shell, through which the proboscis shell, pressed on the right side of the is then extended to eat the bivalve’s fleshy body. mantle cavity, however, and appar- ently interfered with the organs on that side. Accordingly, the gill, auricle, Some snails, such as Bullia and (phylum Cnidaria, Chapter 13) in shal- and kidney of the right side have Buccinum, are scavengers living on low, tropical coral reefs. These snails been lost in most living gastropods, dead and decaying flesh; others are are commonly known as flamingo leading to a condition of bilateral carnivores that tear their prey with tongues. During normal activity their asymmetry. radular teeth. Melongena feeds on brightly colored mantle entirely en- Although loss of the right gill was clams, especially Tagelus, the razor velops the shell, but it can be quickly probably an adaptation to the mechan- clam, thrusting its proboscis between withdrawn into the shell aperture ics of carrying a coiled shell, that con- the gaping shell valves. Fasciolaria when the animal is disturbed. dition displayed in most modern and Polinices (Figure 16-15B) feed on Members of the genus Conus (Fig- prosobranchs made possible a way to a variety of molluscs, preferably bi- ure 16-16) feed on fish, worms, and avoid the problem caused by torsion— valves. Urosalpinx cinerea, oyster bor- molluscs. Their radula is highly modi- fouling. Water is brought into the left ers, drill holes through the shell of fied for prey capture. A gland charges side of the mantle cavity and out the oysters. Their radula, bearing three the radular teeth with a highly toxic right side, carrying with it wastes from longitudinal rows of teeth, is used first venom. When Conus senses the pres- the anus and nephridiopore, which lie to begin the drilling action, then the ence of its prey, a single radular tooth near the right side. Ways in which foul- snails glide forward, evert an accessory slides into position at the tip of the ing is avoided in other gastropods are boring organ through a pore in the proboscis. Upon striking the prey, the mentioned later in the chapter. anterior sole of their foot, and hold it proboscis expels a tooth like a har- against the oyster’s shell, using a poon, and the poison quiets the prey chemical agent to soften the shell. at once. This is an effective adaptation Feeding Habits Short periods of rasping alternate with for a slowly moving predator to pre- Feeding habits of gastropods are as long periods of chemical activity until vent escape of a swiftly moving prey. varied as their shapes and habitats, but a neat round hole is completed. With Some species of Conus can deliver all include use of some adaptation of its proboscis inserted through the hole, very painful stings, and in several the radula. The majority of gastropods a snail may feed continuously for species the sting is lethal to humans. are herbivorous, rasping off particles of hours or days, using its radula to tear The venom consists of a series of toxic algae from hard surfaces. Some herbi- away the soft flesh. Urosalpinx is peptides, and each Conus species car- vores are grazers, some are browsers, attracted to its prey at some distance ries peptides (conotoxins) that are and some are planktonic feeders. Hali- by sensing some chemical, probably specific for the neuroreceptors of its otis, the abalone (Figure 16-15A), holds one released in metabolic wastes of preferred prey. Conotoxins have be- seaweed with its foot and breaks off the prey. come valuable tools in research on the pieces with its radula. Land snails for- Cyphoma gibbosum and related various receptors and ion channels of age at night for green vegetation. species live and feed on gorgonians nerve cells. hic09617_ch16.qxd 5/30/00 12:51 PM Page 336

336 PART 3 The Diversity of Animal Life

A B Figure 16-16 Conus extends its long, wormlike proboscis (A). When a fish attempts to consume this tasty morsel, the Conus stings it in the mouth and kills it. The snail engulfs the fish with its distensible stomach (B), then regurgitates the scales and bones some hours later.

Some gastropods feed on organic through the mantle cavity (in one side cavity RectumMantle deposits on the sand or mud. Others and out the other). collect the same sort of organic debris Pulmonates have a highly vascular Ctenidium (gill) but can digest only the microorganisms area in the mantle that serves as a lung contained in it. Some sessile gastro- (Figure 16-18). Most of the mantle mar- pods, such as some limpets, are ciliary gin seals to the back of the animal, and feeders that use gill cilia to draw in the lung opens to the outside by a Foot particulate matter, roll it into a mucous small opening called a pneumo- A ball, and carry it to their mouth. Some stome. Many aquatic pulmonates must sea butterflies secrete a mucous net to surface to expel a bubble of gas from catch small planktonic forms; then they the lung. To inhale, they curl the edge draw the web into the mouth. of the mantle around the pneu- After maceration by the radula or mostome to form a siphon. by some grinding device, such as a giz- Most gastropods have a single zard in the sea hare Aplysia, digestion nephridium (kidney). The circulatory B is usually extracellular in the lumen of and nervous systems are well devel- the stomach or digestive glands. In cil- oped (Figure 16-18). The latter incor- iary feeders the stomachs are sorting porates three pairs of ganglia con- regions, and most of the digestion is nected by nerves. Sense organs include intracellular in digestive glands. eyes or simple photoreceptors, stato- cysts, tactile organs, and chemorecep- tors. The simplest type of gastropod Internal Form and Function eye is simply a cuplike indentation in Respiration in most gastropods is car- the skin lined with pigmented photore- C ried out by a ctenidium (two ctenidia ceptor cells. In many gastropods the Figure 16-17 is the primitive condition, found in eyecup contains a lens and is covered Evolution of ctenidia in gastropods, A, Primitive some prosobranchs) located in the with a cornea. A sensory area called an condition with two ctenidia and excurrent water mantle cavity, though some aquatic osphradium, located at the base of leaving the mantle cavity by a dorsal slit or hole. B, Condition after one ctenidium had been lost. forms, lacking gills, depend on the the incurrent siphon of most gas- C, Derived condition found in most marine mantle and skin. After the more tropods, is chemosensory in some gastropods, in which filaments on one side of derived prosobranchs lost one of the forms, although its function may be remaining gill are lost, and axis is attached to gills, most of them lost half of the mechanoreceptive in some and is still mantle wall. remaining one, and the central axis unknown in others. became attached to the wall of the There are both dioecious and mantle cavity (Figure 16-17). Thus they monoecious gastropods. Many gas- attained the most efficient gill arrange- tropods perform courtship ceremonies. ment for the way the water circulated During copulation in monoecious hic09617_ch16.qxd 5/30/00 12:51 PM Page 337

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Spermathecal duct rous, brooding their eggs and young in Ovotestis Hermaphroditic Ductus deferens the pallial oviduct. duct Oviduct Intestine Mantle Albumin gland Pulmonary vessels Major Groups of Gastropods Shell (in mantle) Mucous gland Traditional classification of class Gas- Digestive gland Vagina tropoda recognized three subclasses: (liver) Dart sac Prosobranchia, much the largest sub- Stomach Genital Eye class, almost all of which are marine; pore Opisthobranchia, an assemblage includ- Seminal receptacle (spermatheca) Tentacles ing sea slugs, sea hares, nudibranchs, Kidney and canoe shells, all marine; and Pul- Cerebral Heart monata, containing most freshwater ganglion and terrestrial species. Currently, gastro- AnusFoot Excretory Crop Mouth pod taxonomy is in flux. Evidence sug- pore Pedal ganglion gests that Prosobranchia is paraphyletic. PenisSalivary Opisthobranchia may or may not be gland paraphyletic, but Opisthobranchia and Figure 16-18 Pulmonata together apparently form a Anatomy of a pulmonate snail. monophyletic grouping. For conve- nience and organization, we will continue to use the words “proso- branchs” and “opisthobranchs,” recog- nizing that they may not represent valid taxa.

Prosobranchs This group contains most marine snails and some fresh- water and terrestrial gastropods. The mantle cavity is anterior as a result of torsion, with the gill or gills lying in front of the heart. Water enters the left side and exits from the right side, and the edge of the mantle often extends A B into a long siphon to separate incur- rent from excurrent flow. In proso- Figure 16-19 branchs with two gills (for example, Eggs of marine gastropods. A, The wrinkled whelk, Thais lamelosa, lays egg cases resembling grains of wheat; each contains hundreds of eggs. B, Egg ribbon of a dorid nudibranch. the abalone Haliotis and the keyhole limpet Diodora, Figures 16-15A and 16-20A), fouling is avoided by having the excurrent water go up and out species there is an exchange of sper- Fertilized eggs encased in trans- through one or more holes in the shell matozoa or spermatophores (bundles parent shells may be emitted singly to above the mantle cavity. of sperm). Many terrestrial pulmo- float among the plankton or may be Prosobranchs have one pair of ten- nates eject a dart from a dart sac (Fig- laid in gelatinous layers attached to the tacles. Sexes are usually separate. An ure 16-18) into the partner’s body to substratum. Some marine forms en- operculum is often present. heighten excitement before copulation. close their eggs, either in small groups They range in size from periwin- After copulation each partner deposits or in large numbers, in tough egg cap- kles and small limpets (Patella and its eggs in shallow burrows in the sules, or in a wide variety of egg cases Diodora) (Figure 16-20A) to horse ground. Gastropods with the most prim- (Figure 16-19). The young generally conchs (Pleuroploca), the largest gas- itive characteristics discharge ova and emerge as veliger larvae (Figure 16-7), tropods in the Atlantic Ocean. Familiar sperm into seawater where fertilization or they may spend the veliger stage in examples of prosobranchs are occurs, and embryos soon hatch as free- the case or capsule and emerge as abalones (Haliotis), which have an swimming trochophore larvae. In most young snails. Some species, including ear-shaped shell; whelks (Busycon), gastropods fertilization is internal. many freshwater snails, are ovovivipa- which lay their eggs in double-edged, hic09617_ch16.qxd 5/30/00 12:52 PM Page 338

338 PART 3 The Diversity of Animal Life

Figure 16-20 A, Diodora aspera, a gastropod with a hole in its apex through which water leaves the mantle cavity. B, Flamingo tongues, Cyphoma gibbosum, are showy inhabitants of Caribbean coral reefs, where they are associated with gorgonians. These snails have a smooth, creamy, orange to pink shell that is normally covered by the brightly marked mantle.

A B

Rhinophore Oral tentacle

A B Figure 16-21 A, The sea hare, Aplysia dactylomela, crawls and swims across a tropical seagrass bed, assisted by large, winglike parapodia, here curled above the body. B, When attacked, sea hares squirt a copious protective secretion from their “purple gland” in the mantle cavity.

disc-shaped capsules attached to a stones and seaweed; a few are pelagic. Sea hares (Aplysia Figure 16-21), cord a meter long; common periwin- Currently nine or more orders of have large, earlike anterior tentacles kles (Littorina); moon snails (Polinices, opisthobranchs are recognized. and vestigial shells. In pteropods or Figure 16-15B); oyster borers Opisthobranchs show partial or com- sea butterflies (Cavolina and Clione) (Urosalpinx), which bore into oysters plete detorsion; thus the anus and gill the foot is modified into fins for swim- and suck out their juices; rock shells (if present) are displaced to the right ming; thus, they are pelagic and form a (Murex), a European species that was side or rear of the body. Clearly, the part of the plankton fauna. used to make the royal purple of the fouling problem is obviated if the anus Nudibranchs are carnivorous and ancient Romans; and some freshwater is moved away from the head toward often brightly colored (Figure 16-22). forms (Goniobasis and Viviparus). the posterior. Two pairs of tentacles Plumed sea slugs (Aeolidae) which live are usually found, and the second on sea anemones and hydroids, have Opisthobranchs Opisthobranchs pair is often further modified elongate papillae (cerata) covering are an odd assemblage of molluscs (rhinophores, Figure 16-21), with their back. They ingest their prey’s that include sea slugs, sea hares, sea platelike folds that apparently increase nematocysts and transport the nemato- butterflies, and canoe shells. They are the area for chemoreception. Their cysts undischarged to the tips of their nearly all marine; most of them are shell is typically reduced or absent. All cerata. There the nematocysts are shallow-water forms, hiding under are monoecious. placed in cnidosacs that open to the hic09617_ch16.qxd 6/14/00 10:56 PM Page 339

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Zonitoides, Limax, and Agriolimax. Aquatic forms are represented by Heli- soma, Lymnaea, and Physa. Physa is a left-handed (sinistral) snail.

Class Bivalvia (Pelecypoda) Bivalvia are also known as Pelecy- poda (pel-e-sipo-da), or “hatchet- footed” animals, as their name implies (Gr. pelekys, hatchet, pous, podos, foot). They are bivalved molluscs that include mussels, clams, scallops, oys- ters, and shipworms (Figures 16-24 to 16-27) and they range in size from tiny seed shells 1 to 2 mm in length to giant South Pacific clams Tridacna, which Figure 16-22 may reach more than 1 m in length Phyllidia ocellata, a nudibranch. Like other Phyllidia spp., it has a hard body with dense calcareous spicules and bears its gills along the sides, between its mantle and foot. and as much as 225 kg (500 pounds) in weight (see Figure 16-35). Most bivalves are sedentary filter feeders that depend on ciliary currents pro- duced by the gills to bring in food materials. Unlike gastropods, they have no head, no radula, and very little cephalization. Pneumostome Most bivalves are marine, but many live in brackish water and in streams, ponds, and lakes.

Freshwater clams were once abundant and diverse in streams throughout the eastern United States, but they are now easily the most jeopardized group of ani- mals in the country.Of more than 300 species once present, 12 are extinct, 42 A B are listed as threatened or endangered, Figure 16-23 and as many as 88 more may be listed A, Pulmonate land snail. Note two pairs of tentacles; the second, larger pair bears the eyes. soon. A combination of causes is responsi- B, Banana slug, Ariolimax columbianus. Note pneumostome. ble, of which a decline in water quality is among the most important. Pollution and sedimentation from mining, industry,and aquatic species have developed sec- outside, and the aeolid can use its agriculture are among the culprits. Poach- highjacked nematocysts for its own ondary gills in the mantle cavity). The ing to supply the Japanese cultured pearl defense. Hermissenda is one of the anus and nephridiopore open near the industry is partially to blame.And in addi- more common West Coast nudi- pneumostome, and waste is expelled tion to everything else, the prolific zebra branchs. forcibly with air or water from the mussels (see next note) attach in great lung. They are monoecious. Aquatic numbers to the native clams, exhausting Pulmonates Pulmonates show some species have one pair of nonretractile food supplies (phytoplankton) in the sur- detorsion and include land and most tentacles, at the base of which are the rounding water. freshwater snails and slugs (and a few eyes; land forms have two pairs of ten- brackish and saltwater forms). They tacles, with the posterior pair bearing have lost their ancestral ctenidia, but the eyes (Figure 16-23). Among the their vascularized mantle wall has thousands of land species, some of the Form and Function become a lung, which fills with air by most familiar American forms are Shell Bivalves are laterally com- contraction of the mantle floor (some Helix, Polygyra, Succinea, Anguispira, pressed, and their two shells (valves) hic09617_ch16.qxd 5/30/00 12:55 PM Page 340

340 PART 3 The Diversity of Animal Life

A B Figure 16-24 Bivalve molluscs. A, Mussels, Mytilus edulis, occur in northern oceans around the world; they form dense beds in the intertidal zone. A host of marine creatures live protected beneath attached mussels. B, Scallops (Chlamys opercularis) swim to escape attack by starfish (Asterias rubens). When alarmed, these most agile of bivalves swim by clapping the two shell valves together.

of freshwater clams, between the shell and mantle of a certain species of oyster and by keeping the oysters in enclo- sures for several years. Meleagrina is an oyster used extensively by the Japanese for pearl culture.

Body and Mantle The visceral mass is suspended from the dorsal midline, and the muscular foot is attached to the visceral mass anteroventrally. The ctenidia hang down on each side, each covered by a fold of the mantle. The posterior edges of the mantle folds are modified to form dorsal excurrent and ventral incurrent open- Figure 16-25 ings (Figure 16-28A). In some marine Representing a group that has evolved from burrowing ancestors, the surface-dwelling bivalve Pecten sp. has developed sensory organs along its mantle edges (tentacles and a series of blue eyes). bivalves the mantle is drawn out into long muscular siphons that allow the clam to burrow into the mud or sand and extend the siphons to the water above (Figure 16-28B to D). are held together dorsally by a hinge Pearl production is a by-product of ligament that causes the valves to gape a protective device used by the animals Locomotion Bivalves initiate move- ventrally. The valves are drawn to- when a foreign object (grain of sand, ment by extending a slender muscular gether by adductor muscles that work parasite, or other) becomes lodged foot between the valves (Figure 16-28D). in opposition to the hinge ligament between the shell and mantle. The Blood is pumped into the foot, causing (Figure 16-26C and D). The umbo is mantle secretes many layers of nacre it to swell and to act as an anchor in the the oldest part of the shell, and growth around the irritating object (Figure 16-5). mud or sand, then longitudinal muscles occurs in concentric lines around it Pearls are cultured by inserting particles contract to shorten the foot and pull the (Figure 16-26A). of nacre, usually taken from the shells animal forward. hic09617_ch16.qxd 5/30/00 12:57 PM Page 341

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Hinge ligament Excurrent siphonUmbo Anterior end Adductor muscle relaxed

Incurrent siphon Foot A C

Insertion area of Insertion area of Insertion area of anterior adductor muscle anterior retractor posterior adductor muscle

Adductor muscle contracted

B Pallial line Location of siphons D Figure 16-26 Tagelus plebius, stubby razor clam (class Bivalvia). A, External view of left valve. B, Inside of right shell showing scars where muscles were attached. The mantle was attached at the pallial line. C and D, Sections showing function of adductor muscles and hinge ligament. In C, the adductor muscle is relaxed, allowing the hinge ligament to pull the valves apart. In D, the adductor muscle is contracted, pulling the valves together.

A B Figure 16-27 A, Shipworms are bivalves that burrow in wood, causing great damage to unprotected wooden hulls and piers. B, The two small, anterior valves, seen at left, are used as rasping organs to extend the burrow. hic09617_ch16.qxd 6/14/00 11:16 PM Page 342

342 PART 3 The Diversity of Animal Life

Figure 16-28 Adaptations of siphons in bivalves. A, In northwest ugly clams Entodesma saxicola, incurrent and excurrent siphons are clearly visible. B to D, In many marine forms the mantle is drawn out into long siphons. In A, B, and D, the incurrent siphon brings in both food and oxygen. In C, Yoldia, the siphons are respiratory; long ciliated palps feel about over the mud surface and convey food to the mouth.

A

Figure 16-29 Evolution of bivalve ctenidia. By a great lengthening of individual filaments, ctenidia Scallops and file shells are able to incurrent siphon, propelled by ciliary became adapted for filter feeding and separated swim with a jerky motion by clapping action, then enters the water tubes the incurrent chamber from the excurrent, suprabranchial chamber. their valves together to create a sort of through pores between the filaments jet propulsion. The mantle edges can in the lamellae, proceeds dorsally into direct the stream of expelled water, so a common suprabranchial chamber grooves toward the labial palps. The that the animals can swim in virtually (Figure 16-30), and then out the excur- palps, being also grooved and ciliated, any direction (Figure 16-24). rent aperture. direct the mucous mass into the mouth. Some bivalves, such as Nucula Gills Gaseous exchange occurs Feeding Most bivalves are filter feed- and Yoldia, are deposit feeders and through both mantle and gills. Gills of ers. Respiratory currents bring both have long proboscides attached to the most bivalves are highly modified for oxygen and organic materials to the labial palps (Figure 16-28C). These can filter feeding; they are derived from gills where ciliary tracts direct them to be protruded onto sand or mud to col- primitive ctenidia by a great lengthen- the tiny pores of the gills. Gland cells lect food particles, in addition to parti- ing of filaments on each side of the on the gills and labial palps secrete cles attracted by gill currents. central axis (Figure 16-29). As ends of copious amounts of mucus, which Shipworms (Figure 16-27) burrow long filaments became folded back entangles particles suspended in water in wood and feed on particles they exca- toward the central axis, ctenidial fila- going through gill pores. These mucous vate. Symbiotic bacteria live in a special ments took the shape of a long, slen- masses slide down the outside of the organ in the bivalve and produce cellu- der W. Filaments lying beside each gills toward food grooves at the lower lase to digest wood. Other bivalves such other became joined by ciliary junc- edge of the gills (Figure 16-31). Heavier as giant clams gain much of their nutri- tions or tissue fusions, forming plate- particles of sediment drop off the gills tion from the photosynthetic products of like lamellae with many vertical water as a result of gravitational pull, but symbiotic algae living in their mantle tis- tubes inside. Thus water enters the smaller particles travel along the food sue (Figure 16-35). hic09617_ch16.qxd 5/30/00 12:58 PM Page 343

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Ventricle Suprabranchial Adductor muscle water by one or more ships in freshwater chamber ports in northern Europe and then expelled Pericardium between Lake Huron and Lake Erie in 1986. Rectum Mantle This 4 cm bivalve spread throughout the (cut and retracted) Great Lakes by 1990, and by 1994 it was as Auricle far south on the Mississippi as New Excurrent Orleans, as far north as Duluth, Minnesota, Kidney Nonglandular aperture and as far east as the Hudson River in New Glandular York. It attaches to any firm surface and fil- Incurrent ter feeds on phytoplankton. Populations aperture rapidly increase in size. They foul water intake pipes of municipal and industrial Afferent plants, impede intake of water for munici- vessel pal supplies, and have far-reaching effects Efferent on the ecosystem (see preceding note). vessels Zebra mussels will cost billions of dollars to control. Gonad The nervous system consists of three pairs of widely separated ganglia Intestine Gill pores connected by commissures and a sys- Gill bars tem of nerves. Sense organs are poorly Foot developed. They include a pair of stato- Paired gills cysts in the foot, a pair of osphradia of uncertain function in the mantle cav- Mantle Shell ity, tactile cells, and sometimes simple Figure 16-30 pigment cells on the mantle. Scallops Section through heart region of a freshwater clam to show relation of circulatory and respiratory (Pecten, Chlamys) have a row of small systems. Respiratory water currents: water is drawn in by cilia, enters gill pores, and then passes up blue eyes along each mantle edge (Fig- water tubes to suprabranchial chambers and out excurrent aperture. Blood in gills exchanges carbon dioxide for oxygen. Blood circulation: ventricle pumps blood forward to sinuses of foot and viscera, ure 16-25). Each eye has a cornea, lens, and posteriorly to mantle sinuses. Blood returns from mantle to auricles; it returns from viscera to the retina, and pigmented layer. Tentacles kidney, and then goes to the gills, and finally to the auricles. on the margin of the mantle of Pecten (Figure 16-25) and Lima have tactile and Septibranchs, another group of The three-chambered heart, which chemoreceptor cells. bivalves, draw small crustaceans or bits lies in the pericardial cavity (Fig- of organic debris into the mantle cavity ure 16-31), has two auricles and a ven- Reproduction and Development by sudden inflow of water created by tricle and beats slowly, ranging from Sexes are usually separate. Gametes the pumping action of a muscular sep- 0.2 to 30 times per minute. Part of are discharged into the suprabranchial tum in the mantle cavity. the blood is oxygenated in the mantle chamber to be carried out with the and returns to the ventricle through excurrent flow. An oyster may pro- Internal Structure and Function the auricles; the rest circulates duce 50 million eggs in a single sea- The floor of the stomach of filter-feeding through sinuses and passes in a vein son. In most bivalves fertilization is bivalves is folded into ciliary tracts for to the kidneys, from there to the gills external. The embryo develops into sorting a continuous stream of particles. for oxygenation, and back to the trochophore, veliger, and spat stages A cylindrical style sac opening into the auricles. (Figure 16-33). stomach secretes a gelatinous rod called A pair of U-shaped kidneys (ne- In most freshwater clams fertiliza- a crystalline style, which projects into phridial tubules) lies just ventral and tion is internal. Eggs drop into the the stomach and is kept whirling by posterior to the heart (Figure 16-31B). water tubes of the gills where they are means of cilia in the style sac (Fig- The glandular portion of each tubule fertilized by sperm entering with the ure 16-32). Rotation of the style helps to opens into the pericardium; the bladder incurrent flow. They develop there dissolve its surface layers, freeing diges- portion empties into the suprabranchial into a bivalved glochidium larva tive enzymes (especially amylase) that it chamber. stage, which is a specialized veliger contains, and to roll the mucous food (Figure 16-34). When discharged, glo- mass. Dislodged particles are sorted, Zebra mussels,Dreissena polymorpha, are chidia are carried by water currents, and suitable ones are directed to the a recent and disastrous biological introduc- and if they come in contact with a digestive gland or engulfed by amebo- tion into North America. They were appar- passing fish, they attach to its gills or cytes. Further digestion is intracellular. ently picked up as veligers with ballast skin and live as parasites for several hic09617_ch16.qxd 5/30/00 12:59 PM Page 344

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Food in External microscopic teeth that function as very mucous gill effective wood rasps. The animals string extend their burrows with an unceas- A Left mantle ing rasping motion of the valves. This motion sends a continuous flow of fine Mouth wood particles into the digestive tract where they are attacked by cellulase produced by symbiotic bacteria. Inter- estingly, these bacteria also fix nitro- gen, an important property for their hosts, which live on a diet (wood) high Excurrent flow in carbon but deficient in nitrogen. Incurrent flow Some clams bore into rock. The piddock (Pholas) bores into limestone, shale, sandstone, and sometimes wood Incurrent siphon or peat. It has strong valves that bear Palp Foot spines, which it uses to cut away the Shell Sand and debris rock gradually while anchoring itself Right mantle with its foot. Pholas may grow to 15 cm long and make rock burrows up to Nephridiopore Auricle 30 cm long. B Anterior aorta Ventricle Kidney Digestive gland Pericardium Posterior aorta Class Cephalopoda Stomach Rectum Cephalopoda (Gr. kephalƒ, head, pous, podos, foot) include squids, octo- Posterior adductor puses, nautiluses, devilfish, and cuttle- Anterior adductor fish. All are marine, and all are active Anus predators. The modified foot is concentrated Excurrent in the head region. It takes the form of siphon a funnel for expelling water from the Mouth mantle cavity, and the anterior margin Incurrent is drawn out into a circle or crown of siphon arms or tentacles. Cephalopods range upward in size Right gill pair from 2 or 3 cm. The common squid of Mantle markets, Loligo, is about 30 cm long. Foot Intestine The giant squid Architeuthis is the Gonad largest invertebrate known. Figure 16-31 Fossil records of cephalopods go A, Feeding mechanism of freshwater clam. Left valve and mantle are removed. Water enters the back to Cambrian times. The earliest mantle cavity posteriorly and is drawn forward by ciliary action to the gills and palps. As water enters shells were straight cones; others were the tiny openings of the gills, food particles are sieved out and caught in strings of mucus that are carried by cilia to the palps and directed to the mouth. Sand and debris drop into the mantle cavity curved or coiled, culminating in the and are removed by cilia. B, Clam anatomy. coiled shell similar to that of the mod- ern Nautilus, the only remaining mem- ber of the once flourishing nautiloids weeks. Then they sink to the bottom to Teredo, Bankia, and some other (Figure 16-36). Cephalopods without begin independent lives. Larval “hitch- genera are called shipworms. They can shells or with internal shells (such hiking” helps distribute a form whose be very destructive to wooden ships as octopuses and squids) apparently locomotion is very limited. and wharves. These strange little clams evolved from some early straight- have a long, wormlike appearance, shelled ancestor. Many ammonoids, Boring Many pelecypods can bur- with a pair of slender posterior siphons which are extinct, had quite elaborate row into mud or sand, but some have that keep water flowing over the gills, shells (Figure 16-36C). evolved a mechanism for burrowing and a pair of small globular valves on The natural history of some ceph- into much harder substances, such as the anterior end with which they bur- alopods is fairly well known. They are wood or stone. row (Figure 16-27). The valves have marine animals and appear sensitive to hic09617_ch16.qxd 5/30/00 1:00 PM Page 345

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Digestive glands the degree of salinity. Few are found in the Baltic Sea, where the water has Esophagus a low salt content. Cephalopods are Style found at various depths. Octopuses sac Typhlosole Gastric are often seen in the intertidal zone, shield lurking among rocks and crevices, but A Rotating occasionally they are found at great Typhlosole mucus-food cord depths. The more active squids are Stomach rarely found in very shallow water, and Rotating crystalline some have been taken at depths of style 5000 m. Nautilus is usually found near Esophagus Intestine the bottom in water 50 to 560 m deep, Sorting Small food particles near islands in the southwestern area carried to digestive Pacific. gland B Large particles passed to intestine The enormous giant squid, Architeuthis, is Cilia very poorly known because no one has Typhlosole C ever been able to study a living specimen. Figure 16-32 The anatomy has been studied from strand- Stomach and crystalline style of ciliary-feeding clam. A, External view of stomach and style sac. ed animals, from those captured in nets of B, Transverse section showing direction of food movements. Food particles in incoming water are fishermen, and from specimens found in caught in a cord of mucus that is kept rotating by the crystalline style. Ridged sorting areas direct the stomach of sperm whales.The mantle large particles to the intestine and small food particles to digestive glands. C, Sorting action of cilia. length is 5 to 6 m, and the head is up to one meter.They have the largest eyes in the ani- mal kingdom: up to 25 cm (10 inches) in diameter.They apparently eat fish and other Shell squids, and they are an important food item Egg for sperm whales.They are thought to live on or near the sea bottom at a depth of 1000 m, but some have been observed Trochophore swimming at the surface. larva Cilia Brain Mouth Stomach Form and Function Mantle Gonad Shell Although early nautiloid and Intestine Adductor ammonoid shells were heavy, they muscle were made buoyant by a series of gas Adult oyster Anus Valve chambers, as is that of Nautilus (Fig- Gill ure 16-36B), enabling the animal to Shell swim while carrying its shell. The shell of Nautilus, although coiled, is quite Adult oyster different from that of a gastropod. The shell is divided by transverse septa into internal chambers (Figure 16-36B). The living animal inhabits only the last Foot chamber. As it grows, it moves for- Veliger ward, secreting behind a new septum. larva The chambers are connected by a cord of living tissue called a siphuncle, which extends from the visceral mass. Spat Cuttlefishes (Figure 16-37) also have a small, curved shell, but it is entirely enclosed by the mantle. In squids most Figure 16-33 of the shell has disappeared, leaving Life cycle of oysters. Oyster larvae swim about for approximately 2 weeks before settling down for only a thin, horny strip called a pen, attachment to become spats. Oysters take about 4 years to grow to commercial size. which is enclosed by the mantle. In hic09617_ch16.qxd 5/30/00 1:00 PM Page 346

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Octopus (Gr. oktos, eight, pous, podos, foot) the shell has disappeared entirely.

Locomotion Cephalopods swim by forcefully expelling water from the mantle cavity through a ventral funnel (or siphon)—a sort of jet propulsion. The funnel is mobile and can be pointed forward or backward to con- trol direction; the force of water expul- sion controls speed. Squids and cuttlefishes are excel- lent swimmers. The squid body is A B streamlined and built for speed (Fig- Figure 16-34 ure 16-38). Cuttlefishes swim more A, Glochidium, or larval form, for some freshwater clams. When larvae are released from brood pouch slowly. The lateral fins of squids and of mother, they may become attached to a fish’s gill by clamping their valves closed. They remain as parasites on the fish for several weeks. Their size is approximately 0.3 mm. B, Some clams have cuttlefishes serve as stabilizers, but adaptations that help their glochidia find a host. The mantle edge of this female pocketbook mussel they are held close to the body for (Lampsilis ovata) mimics a small minnow, complete with eye. When a smallmouth bass comes to dine, rapid swimming. it gets doused with glochidia. Nautilus is active at night; its gas- filled chambers keep the shell upright. Although not as fast as squids, it moves surprisingly well. Octopus has a rather globular body and no fins (Figure 16-1E). An octopus can swim backward by spurting jets of water from its funnel, but it is better adapted to crawling about over the rocks and coral, using suction discs on its arms to pull or to anchor itself. Some deep-water octopods have the arms webbed like an umbrella and swim in a medusa-like fashion.

Internal Features The active habits of cephalopods are reflected in their internal anatomy, particularly their respiratory, circulatory, and nervous systems.

Respiration and Circulation. Except for nautiloids, cephalopods have one pair of gills. Because ciliary propulsion would not circulate enough water for their high oxygen requirements, there are no cilia on the gills. Instead, radial muscles in the mantle wall compress the wall and enlarge the mantle cavity, drawing water inside. Strong circu- lar muscles contract and expel water forcibly through the funnel. A system Figure 16-35 of one-way valves prevents water from Clam (Tridacna gigas) lies buried in coral rock with greatly enlarged siphonal area visible. These tissues are richly colored and bear enormous numbers of symbiotic single-celled algae (zooxanthellae) that being taken in through the funnel and provide much of the clam’s nutriment. expelled around the mantle margin. hic09617_ch16.qxd 6/14/00 11:18 PM Page 347

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Figure 16-36 problem was solved by the develop- Nautilus, a cephalopod. A, Live Nautilus, feeding ment of accessory or branchial hearts on a fish. B, Longitudinal section, showing gas- (Figure 16-38B) at the base of each gill filled chambers of shell, and diagram of body to increase the pressure of the blood structure. C, Longitudinal section through shell of an ammonoid. going through the capillaries there.

After Nautilus secretes a new septum, the new chamber is filled with fluid similar in ionic composition to that of the Nautilus’ blood (and of seawater). Fluid removal A involves the active secretion of ions into tiny intercellular spaces in the siphuncular epithelium, so that a very high local os- motic pressure is produced, and water is drawn out of the chamber by osmosis. The gas in the chamber is just the respiratory gas from the siphuncle tissue that diffuses into the chamber as fluid is removed. Thus the gas pressure in the chamber is 1 atmo- sphere or less because it is in equilibrium with the gases dissolved in the seawater surrounding the Nautilus, which are in turn in equilibrium with air at the surface of the sea, despite the fact that the Nautilus may be swimming at 400 m beneath the surface.That the shell can withstand implo- sion by the surrounding 41 atmospheres (about 600 pounds per square inch), and B that the siphuncle can remove water against this pressure are marvelous feats of natural engineering!

Nervous and Sensory Systems. Nervous and sensory systems are more elaborate in cephalopods than in other molluscs. The brain, the largest in any inverte- brate, consists of several lobes with mil- lions of nerve cells. Squids have giant nerve fibers (among the largest known in the animal kingdom), which are acti- vated when the animal is alarmed and that initiate maximal contractions of the mantle muscles for a speedy escape. Sense organs are well developed. Except for Nautilus, which has rela- tively simple eyes, cephalopods have highly complex eyes with cornea, lens, C chambers, and retina (Figure 16-39). Orientation of the eyes is controlled by the statocysts, which are larger and Likewise, the open circulatory sys- thermore, the molluscan plan of circula- more complex than in other molluscs. tem of their ancestral molluscs would be tion places the entire systemic circula- The eyes are held in a constant rela- inadequate for cephalopods. Their cir- tion before the blood reaches the gills tion to gravity, so that the slit-shaped culatory system consists of a closed net- (in contrast to vertebrates, in which the pupils are always in a horizontal posi- work of vessels, and capillaries conduct blood leaves the heart and goes directly tion. Octopods are apparently color- blood through the gill filaments. Fur- to the gills or lungs). This functional blind but can be taught to discriminate hic09617_ch16.qxd 6/15/00 7:58 AM Page 348

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between shapes—for example, a square and a rectangle—and to remember such a discrimination for a considerable time. Experimenters find it easy to modify their behavior patterns by devices of re- ward and punishment. They are capable of observational learning; when one octopus observes another being re- warded by making a correct choice, the observer learns which choice is rewarded and consistently makes the same selection when given the opportunity. Octopods use their arms for tactile exploration and can discriminate between textures by feel but appar- ently not between shapes. Their arms are well supplied with both tactile and Figure 16-37 chemoreceptor cells. Cephalopods Cuttlefish, Sepia latimanus, has an internal shell familiar to keepers of caged birds as “cuttlebone.” seem to lack a sense of hearing.

Communication Little is known of social behavior of nautiloids or deep- water cephalopods, but inshore and lit- toral forms such as Sepia, Sepioteuthis, Loligo, and Octopus have been studied extensively. Although their tactile sense is well developed and they have some chemical sensitivity, visual sig- nals are the predominant means of communication. These signals consist of a host of movements of the arms, fins, and body, as well as many color changes. The movements may range A from minor body motions to exagger- ated spreading, curling, raising, or low- Anterior aorta ering of some or all of the arms. Color Digestive gland Salivary changes are effected by chro- BrainArm gland and Esophagus Stomach Mantle artery matophores, cells in the skin that con- duct Kidney Cecum Jaw tain pigment granules. Tiny muscle Mantle cells surround each elastic chro- Pen matophore, whose contractions pull the cell boundary of the chro- matophore outward, causing it to expand greatly. As the cell expands, the pigment becomes dispersed, Gonad Radula changing the color pattern of the ani- Anus Gill Intestine Gill Systemic Posterior Statocyst mal. When the muscles relax, the chro- Funnel heart heart vena cava Ink sac matophores return to their original size with Gonoduct valve and pigment becomes concentrated again. By means of the chro- matophores, which are under nervous B and probably hormonal control, an Tentacle elaborate system of changes in color Figure 16-38 and pattern is possible, including gen- A, Reef squid Sepioteuthis lessoniana. B, Lateral view of squid anatomy, with the left half of the eral darkening or lightening; flushes of mantle removed. pink, yellow, or lavender; and the hic09617_ch16.qxd 5/30/00 1:08 PM Page 349

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directions, and it can instantaneously change any or all of the messages. Probably no other system of communi- cation in invertebrates can convey so much information so rapidly. Deep-water cephalopods may have to depend more on chemical or tactile senses than their littoral or surface cousins, but they also produce their own type of visual signals, for they have evolved many elaborate lumines- cent organs. Most cephalopods other than nau- tiloids have another protective device. An ink sac that empties into the rectum contains an ink gland that secretes sepia, a dark fluid containing the pig- ment melanin, into the sac. When the animal is alarmed, it releases a cloud of ink, which may hang in the water as a blob or be contorted by water currents. The animal quickly departs from the scene, leaving the ink as a decoy to the predator.

Figure 16-39 Eye of a cuttlefish (Sepia). The structure of cephalopod eyes shows a high degree of convergent Reproduction Sexes are separate in evolution with eyes of vertebrates. cephalopods. In the male seminal vesicle the spermatozoa are encased in spermatophores and stored in a sac that opens into the mantle cavity. One arm of the adult male is modified as an intromittent organ, called a hecto- cotylus, used to pluck a sper- A matophore from his own mantle cav- ity and insert it into the mantle cavity of a female near the oviduct opening (Figure 16-40). Before copulation males often undergo color displays, apparently directed against rival males. Eggs are fertilized as they leave the oviduct and are then usually attached to stones or other objects. Some octopods tend their eggs. Arg- B onauta, the paper nautilus, secretes a fluted “shell,” or capsule, in which she broods her eggs. Figure 16-40 The large yolky eggs undergo Copulation in cephalopods. A, Mating cuttlefishes. B, Male octopus uses modified arm to deposit meroblastic cleavage. During embry- spermatophores in female mantle cavity to fertilize her eggs. Octopuses often tend their eggs during onic development, the head and foot development. become indistinguishable. The ring around the mouth, which bears the formation of bars, stripes, spots, or By assuming different color pat- arms, or tentacles, may be derived irregular blotches. These colors may be terns of different parts of the body, from the anterior part of the foot. used variously as danger signals, as a squid can transmit three or four A juvenile hatches from the egg; protective coloring, in courtship rituals, different messages simultaneously to no free-swimming larva exists in and probably in other ways. different individuals and in different cephalopods. hic09617_ch16.qxd 6/14/00 11:19 PM Page 350

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Major Groups of Cephalopods squids are stalked (pendunculated), rarely leave recognizable fossils. Therefore with horny rims bearing teeth; in octo- we have no record of molluscs before they There are three subclasses of ceph- had shells, and there can be some doubt alopods: Nautiloidea, which have two puses the suckers are sessile and have no horny rims. that certain early fossil shells are really pairs of gills; the entirely extinct remains of molluscs, particularly if the Ammonoidea; and Coleoidea, which group they represent is now extinct.The have one pair of gills. Nautiloidea pop- Phylogeny and issue of how to define a mollusc from hard ulated the Paleozoic and Mesozoic seas, parts alone was emphasized by Yochelson but there survives only one genus, Nau- Adaptive Radiation (1978, Malacologia 17:165), who said,“If tilus (see Figure 16-36), of which there scaphopods were extinct and soft parts The first molluscs probably arose dur- are five or six species. Nautilus’ head, were unknown, would they be called mol- ing Precambrian times because fossils with its 60 to 90 or more tentacles, can lusks? I think not.” attributed to Mollusca have been found be extended from the opening of the in geological strata as old as the early body compartment of the shell. Its ten- A “hypothetical ancestral mollusc” Cambrian period. On the basis of such tacles have no suckers but are made (see Figure 16-2) was long viewed as shared features as spiral cleavage, adhesive by secretions. They are used representing the original mollusc an- mesoderm from the 4d blastomere, and in searching for, sensing, and grasping cestor, but neither a solid shell nor a trochophore larva, most zoologists have food. Beneath its head is the funnel. broad, crawling foot are now consid- accepted Mollusca as protostomes, Mantle, mantle cavity, and visceral mass ered universal characters for Mollusca. allied with the annelids and arthropods. are sheltered by the shell. The primitive ancestral mollusc was Opinions differ, however, as to whether Ammonoids were widely preva- probably a more or less wormlike molluscs were derived from a flatworm- lent in the Mesozoic era but became organism with a ventral gliding surface like ancestor independent of annelids, extinct by the end of the Cretaceous and a dorsal mantle with a chitinous share an ancestor with annelids after period. They had chambered shells cuticle and calcareous scales (Fig- the advent of the coelom, or share a analogous to nautiloids, but the septa ure 16-41). It had a posterior mantle metameric common ancestor with were more complex, and the septal cavity with two gills, a radula, a ladder- annelids. This last hypothesis is sutures (where the septa contact the like nervous system, and an open strengthened if Neopilina (class Mono- inside of the shell) were frilled (com- circulatory system with a heart. Among placophora) can be considered pare shells in Figure 16-36B and C). living molluscs the primitive condition metameric, as some scientists have con- The reasons for their extinction is most nearly approached by caudo- tended. However, it is unlikely that remain a mystery. Present evidence foveates, although the foot is reduced such a successful adaptation as suggests that they were gone before to an oral shield in members of this metamerism would have been lost in all the asteroid bombardment at the end class. Solenogasters have lost the gills, later molluscs, and there is no trace of of the Cretaceous period (p. 132), and the foot is represented by the ven- metamerism in development of any and some nautiloids, which some tral groove. Both these classes proba- known molluscan larva. Therefore most ammonoids closely resembled, sur- bly branched from primitive ancestors zoologists now suggest that the replica- vive to the present. before the development of a solid tion of body parts found in the mono- Subclass Coleoidea includes all liv- shell, a distinct head with sensory placophorans is pseudometamerism. ing cephalopods except Nautilus. organs, and the ventral muscularized The most reasonable hypothesis is that There are four orders of coleoids. foot. Polyplacophorans probably also molluscs branched off from the annelid Members of order Sepioidea (cuttle- branched early from the main lines of line after the coelom arose but before fishes and their relatives) have a molluscan evolution before the veliger the advent of metamerism. Some analy- rounded or compressed, bulky body was established as the larva. Some ses suggest that molluscs and annelids bearing fins (Figure 16-37). They have workers believe that shells of polypla- are more closely related to each other eight arms and two tentacles. Both cophorans are not homologous to than either is to the arthropods. This arms and tentacles have suckers, but shells of other molluscs because they contention is strengthened by molecu- tentacles bear suckers only at their differ structurally and developmentally. lar evidence that places annelids and ends (Figure 16-37). Members of order Polyplacophora and the remaining molluscs in Lophotrochozoa and arthro- Teuthoidea (squids, Figure 16-38) have classes are sister groups (Figure 16-42). pods in Ecdysozoa (p. 209). a more cylindrical body but also have Some investigators believe that eight arms and two tentacles. Order Gastropoda are polyphyletic, perhaps being composed of several groups Vampyromorpha (vampire squid) con- Fossils are remains of past life uncovered tains only a single, deep-water species. from the crust of the earth (Chapter 6). independently derived from an ances- Members of order Octopoda have They can be actual parts or products of ani- tor shared with monoplacophorans, eight arms and no tentacles (see Fig- mals (teeth, bones, shells, and so on), petri- but cladistic analysis suggests that ure 16-1E). Their bodies are short and fied skeletal parts, molds, casts, impressions, Gastropoda and Cephalopoda form the saclike, with no fins. The suckers in footprints, and others. Soft and fleshy parts sister group to Monoplacophora (see hic09617_ch16.qxd 5/30/00 1:09 PM Page 351

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Monoplacophora

Gastropoda Cephalopoda

Scaphopoda

Bivalvia

Polyplacophora

Solenogastres

Caudofoveata

PRESENTCENOZOICMESOZOICPALEOZOICPRECAMBRIAN

Figure 16-41 Classes of Mollusca, showing their derivations and relative abundance.

Figure 16-42). Both gastropods and substratum and their ability to swim. spatulate foot and reduction of the cephalopods have a greatly expanded Development of their respiratory, cir- head and sense organs. visceral mass. The mantle cavity was culatory, and nervous systems is corre- Most diversity among molluscs is brought toward the head by torsion in lated with their predatory and swim- related to their adaptation to different gastropods, but in cephalopods the ming habits. habitats and modes of life and to a mantle cavity was extended ventrally. Scaphopods and bivalves have an wide variety of feeding methods, rang- Evolution of a chambered shell in expanded mantle cavity that essentially ing from sedentary filter feeding to cephalopods was a very important envelops the body. Adaptations for active predation. There are many adap- contribution to their freedom from the burrowing characterize this clade: the tations for food gathering within the hic09617_ch16.qxd 5/30/00 1:09 PM Page 352

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Mollusca

Caudofoveata Solenogastres Polyplacophora Monoplacophora Gastropoda Cephalopoda Bivalvia Scaphopoda Torsion Byssus Further concentration Loss of radula of visceral mass Bivalve shell Siphuncle Lateral compression Beaklike jaws of body Arms/tentacles and siphon Univalve, caplike shell Septate shell Captacula Loss of gills Serial repetition of soft parts Closed circulatory system Foot groove Loss of gills Copulatory spicules Tusk-shaped, open- at posterior Shell coiling ended shell Well-developed head Viscera concentrated dorsally Dorsoventrally elongated body

Unique shell with 7–8 plates Mantle cavity extended Nervous system decentralized along sides of foot Head reduced Multiple gills Spatulate foot Expansion of mantle cavity Calcareous spicules to surround body form scales

Single, well-defined shell gland Periostracum, prismatic and nacreous layers Shell univalve

Multiple foot retractor muscles Preoral tentacles Large, muscular foot Concentration of shell gland to produce solid shell(s)

Posterior mantle cavity with 1 or more pairs of gills Radula Chambered heart with atria and ventricle Muscular foot (or foot precursor) Calcareous spicules produced by mantle shell gland Mantle Reduction of coelom and development of hemocoel

Figure 16-42 Cladogram showing hypothetical relationships among classes of Mollusca. Synapomorphies that identify the various clades are shown, although a number of these have been modified or lost in some descendants. For example, the univalve shell (as well as shell coiling) has been reduced or lost in many gastropods and cephalopods, and many gastropods have undergone detorsion. The bivalve shell of the Bivalvia was derived from an ancestral univalve shell. The byssus is not present in most adult bivalves but functions in larval attachment in many; therefore the byssus is considered a synapomorphy of Bivalvia. Source: Modified from R. C. Brusca, Invertebrates. Sinauer Associates, Inc., Sunderland, MA, 1990.

phylum and an enormous variety in capacity than any other molluscan times functions in locomotion, in the radular structure and function, particu- structure. Besides secreting the shell feeding processes, or in a sensory larly among gastropods. and forming the mantle cavity, it is var- capacity. The shell, too, has undergone The versatile glandular mantle has iously modified into gills, lungs, a variety of evolutionary adaptations. probably shown more plastic adaptive siphons, and apertures, and it some- hic09617_ch16.qxd 5/30/00 1:10 PM Page 353

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Classification of Phylum large coelomic cavities; radula pres- gills or a lung; most with single auri- Mollusca ent; six pairs of nephridia, two of cle and single nephridium; nervous which are gonoducts; separate sexes. system with cerebral, pleural, pedal, Useful characteristics for distinction of Example: Neopilina (see Figure 16-8). and visceral ganglia; dioecious or classes of molluscs are type of foot and Class Polyplacophora (poly-pla-kof monoecious, some with trochophore, type of shell. Several other characteristics o-ra) (Gr. polys, many, several, typically with veliger, some without are important in particular classes. plax, plate, phora, bearing): chi- pelagic larva. Examples: Busycon, Class Caudofoveata (kaw do-fo-ve-at tions. Elongated, dorsoventrally flat- Polinices (see Figure 16-15B), Physa, a) (L. cauda, tail, fovea, small pit). tened body with reduced head; bilat- Helix, Aplysia (see Figure 16-21). Wormlike; shell, head, and excretory erally symmetrical; radula present; Class Bivalvia (bi-valve-a) (L. bi, organs absent; radula usually present; shell of eight dorsal plates; foot broad two, valva, folding door, valve) mantle with chitinous cuticle and cal- and flat; gills multiple along sides of (Pelecypoda): bivalves. Body careous scales; oral pedal shield near body between foot and mantle edge; enclosed in a two-lobed mantle; shell anterior mouth; mantle cavity at pos- sexes usually separate, with a trocho- of two lateral valves of variable size terior end with pair of gills; sexes phore but no veliger larva. Examples: and form, with dorsal hinge; head separate; formerly united with Mopalia (see Figure 16-10), Tonicella greatly reduced, but mouth with labial solenogasters in Class Aplacophora. (see Figure 16-1A). palps; no radula; no cephalic eyes, a Examples: Chaetoderma, Limifossor. Class Scaphopoda (ska-fopo-da) few with eyes on mantle margin; foot Class Solenogastres (so-len o-gas (Gr. skaphƒ, trough, boat, pous, usually wedge shaped; gills platelike; trez) (Gr. solen, pipe, gaster, stom- podos, foot): tusk shells. Body sexes usually separate, typically with ach): solenogasters. Wormlike; shell, enclosed in a one-piece tubular shell trochophore and veliger larvae. head, and excretory organs absent; open at both ends; conical foot; Examples: Anodonta, Venus, Tagelus radula present or absent; mantle usu- mouth with radula and tentacles; (see Figure 16-26), Teredo (see ally covered with scales or spicules; head absent; mantle for respiration; Figure 16-27). mantle cavity posterior, without true sexes separate; trochophore Class Cephalopda (sefa-lopo-da) gills, but sometimes with secondary larva. Example: Dentalium (see (Gr. kephalƒ, head, pous, podos, respiratory structures; foot repre- Figure 16-11). foot): squids and octopuses. Shell sented by long, narrow, ventral pedal Class Gastropoda (gas-tropo-da) often reduced or absent; head well groove; hermaphroditic. Example: (Gr. gaster, stomach, pous, podos, developed with eyes and a radula; Neomenia. foot): snails and slugs. Body asym- head with arms or tentacles; foot Class Monoplacophora (mon o-pla- metrical and shows effects of torsion; modified into siphon; nervous system kof o-ra) (Gr. monos, one, plax, body usually in a coiled shell (shell of well-developed ganglia, centralized plate, phora, bearing). Body bilat- uncoiled or absent in some); head to form a brain; sexes separate, with erally symmetrical with a broad flat well developed, with radula; foot direct development. Examples: Loligo foot; a single limpetlike shell; mantle large and flat; one or two gills, or (see Figure 16-38), Octopus (see Fig- cavity with five or six pairs of gills; with mantle modified into secondary ure 16-1E), Sepia (see Figure 16-37).

Summary

Mollusca is one of the largest and most the animals that have it, an efficient hydro- system of molluscs is open, with a heart diverse phyla, its members ranging in size static skeleton. and blood sinuses. Molluscs usually have a from very small organisms to the largest of The mantle and mantle cavity are pair of nephridia connecting with the invertebrates. Their basic body divisions important characteristics of molluscs. The coelom and a complex nervous system are head, foot, and visceral mass, which is mantle secretes the shell and overlies a part with a variety of sense organs. The primi- usually covered by a shell. The majority are of the visceral mass to form a cavity hous- tive larva of molluscs is the trochophore, marine, but some are freshwater, and a few ing the gills. The mantle cavity has been and most marine molluscs have a more are terrestrial. They occupy a wide variety modified into a lung in some molluscs. The advanced larva, the veliger. of niches. A number are economically foot is usually a ventral, solelike, locomo- Classes Caudofoveata and Solenogas- important, and a few are medically impor- tory organ, but it may be variously modi- tres are small groups of wormlike molluscs tant as hosts of parasites. fied, as in cephalopods, where it has with no shell. Scaphopoda is a slightly Molluscs are coelomate (have a coe- become arms and a funnel. The radula is larger class with a tubular shell, open at lom), although their coelom is limited to found in all molluscs except bivalves and both ends, and the mantle wrapped around the area around the heart and gonads. Evo- solenogasters and is a protrusible, tongue- the body. lutionary development of a coelom was like organ with teeth used in feeding. Class Monoplacophora is a tiny, uni- important because it enabled better organi- Except in cephalopods, which have a valve marine group showing pseudometam- zation of visceral organs and, in many of closed circulatory system, the circulatory erism. Polyplacophora are more common, hic09617_ch16.qxd 5/30/00 1:10 PM Page 354

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marine organisms with shells in the form of in various ways among different gas- most advanced molluscs; they are all a series of eight plates. They are rather tropods. Among the solutions to fouling are predators and many can swim rapidly. sedentary animals with a row of gills along bringing water into one side of the mantle Their tentacles capture prey by adhesive each side of their foot. cavity and out the other (many gastro- secretions or by suckers. They swim by Gastropoda are the most successful pods), some degree of detorsion (opistho- forcefully expelling water from their mantle and largest class of molluscs. Their interest- branchs), and conversion of the mantle cavity through a funnel, which was derived ing evolutionary history includes torsion, or cavity into a lung (pulmonates). from the foot. the twisting of the posterior end to the Class Bivalvia are marine and fresh- There is strong embryological evi- anterior, so that anus and head are at the water, and they have their shell divided dence that molluscs share a common same end, and coiling, an elongation and into two valves joined by a dorsal ligament ancestor with annelids more recently than spiraling of the visceral mass. Torsion has and held together by an adductor muscle. either of these phyla do with arthropods or led to the problem of fouling, which is the Most of them are filter feeders, drawing deuterostome phyla, although the molluscs release of excreta over the head and in water through their gills by ciliary action. are not metameric. front of the gills, and this has been solved Members of class Cephalopoda are the

Review Questions

1. Members of such a large and diverse nacreous layer, metanephridia, 12. How is the ctenidium modified from phylum as Mollusca impact humans in nephrostome, trochophore, veliger, the ancestral form in a typical bivalve? many ways. Discuss this statement. glochidium, osphradium. 13. What is the function of the siphuncle 2. How does the coelom develop embry- 6. Briefly describe the habitat and habits of cephalopods? ologically? Why was the evolutionary of a typical chiton. 14. Describe how cephalopods swim and development of a coelom important? 7. Define the following with respect to how they eat. 3. What are characteristics of Mollusca gastropods: operculum, columella, tor- 15. Describe adaptations in the circulatory that distinguish it from other phyla? sion, fouling, bilateral asymmetry, and neurosensory systems of 4. Briefly describe characteristics of the rhinophore, pneumostome. cephalopods that are particularly valu- ancestral mollusc, and tell how each 8. What survival problem did torsion cre- able for actively swimming, preda- class of molluscs (Caudofoveata, ate? How have gastropods evolved to ceous animals. Solenogastres, Monoplacophora, Poly- avoid this problem? 16. Distinguish between ammonoids and placophora, Scaphopoda, Gastropoda, 9. Gastropods have radiated enormously. nautiloids. Bivalvia, Cephalopoda) differs from Illustrate this statement by describing 17. Which other invertebrate groups are the ancestral condition with respect to variations in feeding habits found in likely to be the closest relatives of each of the following: shell, radula, gastropods. molluscs? What is the evidence for the foot, mantle cavity and gills, circula- 10. Distinguish among opisthobranchs and relationship? tory system, and head. pulmonates. 5. Define the following: ctenidia, odon- 11. Briefly describe how a typical bivalve tophore, periostracum, prismatic layer, feeds and how it burrows.

Selected References

Barinaga, M. 1990. Science digests the secrets of Houghton Mifflin Company. An excellent Ross, J. 1994. An aquatic invader is running voracious killer snails. Science 249:250–251. revision of a popular handbook. amok in U.S. waterways. Smithsonian Describes current research on the toxins Moynihan, M. 1985. Communication and non- 24(11):40–50 (Feb.). A small bivalve, the produced by cone snails. communication by cephalopods. Bloom- zebra mussel apparently introduced into Gosline, J. M., and M. D. DeMont. 1985. Jet- ington, Indiana University Press. Readable the Great Lakes with ballast water from propelled swimming in squids. Sci. Am. summarization of our understanding of ships, is clogging up intake pipes and 252:96–103 (Jan.). Mechanics of swimming communication in this remarkable group municipal water supplies. It will take bil- in squid are analyzed; elasticity of collagen of molluscs. lions of dollars to control. in mantle increases efficiency. Roper, C. R. E., and K. J. Boss. 1982. The giant Ward, P. 1983. The extinction of the ammonites. Kuznik, F. 1993. America’s aching mussels. squid. Sci. Am. 246:96–105 (April). Many Sci. Am. 249:136–147 (Oct.). Like nau- National Wildlife (Oct.–Nov.) pp. 34–39. mysteries remain about the deep-sea squid, tiloids, ammonoids arose in the Paleozoic. Details the miserable status of freshwater Architeuthis, because it has never been Subsequently, they underwent several clams (or mussels) in the United States. studied alive. It can reach a weight of explosive radiations, the last of which was Morris, P. A. (W. J. Clench [editor]). 1973. A field 1000 pounds and a length of 18 m, and its in the late Mesozoic, and then became guide to shells of the Atlantic and Gulf eyes are as large as automobile headlights. extinct. coasts and the West Indies, ed. 3. Boston, hic09617_ch16.qxd 6/14/00 11:20 PM Page 355

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Ward, P., L. Greenwald, and O. E. Greenwald. host snail Biomphalaria glabrata (Gas- neotropical ones. Thus, when S. mansoni 1980. The buoyancy of the chambered tropoda: Planorbidae). Biol. J. Linn. Soc. was brought to New World in African nautilus. Sci. Am. 243:190–203 (Oct.). 60:505–516. The pulmonate snail Biom- slaves, it found a compatible host. Reviews discoveries on how the nautilus phalaria glabrata is the intermediate host in Zorpette, G. 1996. Mussel mayhem, continued. removes water from a chamber after secret- the New World for Schistosoma mansoni, Sci. Am. 275:22–23 (Aug.). Some benefits, ing a new septum. an important trematode of humans (p. 290). though dubious, of the zebra mussel inva- Woodruff, D. S., and M., Mulvey. 1997. Neotrop- Allozyme analysis shows that B. glabrata sion have been described, but these are out- ical schistosomiasis: African affinities of the clusters with African species rather than the weighted by the problems created.

Zoology Links to the Internet

Visit the textbook’s web site at Phylum Mollusca, from the University of Cephalopoda. Information and links and www.mhhe.com/zoology to find live Minnesota. many references on cephalopods. Internet links for each of the references Molluscs. Keys to Marine Invertebrates of Class Cephalopoda. below. the Woods Hole Region. Descriptive infor- Dissection of the Squid. Terrific photos of Animal Diversity Web, University of mation, definition of terminology, and external and internal organs (loads slowly); Michigan. Phylum Mollusca. Information keys to the bivalves and gastropods of the some pictures are labeled, others are not. on molluscs, and links to all seven classes Woods Hole Region. Separate pictures of various aspects of of molluscs. Some images may not be Clam Dissection. University of Minnesota. external anatomy, individual pictures of displayed due to copyright restrictions. Nice photograph of internal anatomy, but various internal organs or organ systems. Mollusca. Arizona’s Tree of Life Web Page. not labeled. Squid Dissection. This lesson plan was Pictures, characteristics, phylogenetic rela- Cephalopod Page. Information and images actually designed for students in grade 2, tionships, references on molluscs. Pictures of cephalopods. but there are some interesting facts! and references, and links to polypla- cophorans, gastropods, bivalves, and cephalopods. Most sites have reference lists.