Number of families Approximately 120
Mainly terrestrial but also freshwater and marine slugs and snails, almost all having an enclosed lung
Photo: A garden snail (Helix aspersa) issuing defensive "foam." (Photo by Holt Studios, Int./Photo Researchers, Inc. Reproduced by permission.)
Evolution and systematics
The earliest fossil pulmonate land snails date back over 300 million years to the Carboniferous period of North America and Europe, although there is some controversy as to whether these belong to primitive pulmonate families such as the Ellobiidae, or to more advanced families of the major terrestrial pulmonate group Stylommatophora. The first certain stylommatophoran fossils date from the Lower Cretaceous (about 140 million years ago [mya]), and become more common during the Upper Cretaceous, with several genera attributable to modern families such as the Plectopylidae, Streptaxidae, and Camaenidae present. Most extant families appear in the fossil record for the first time during the Ceno-zoic era (from 65 mya).
The subclass Pulmonata evolved from opisthobranch (marine gastropod mollusks of the subclass Opisthobranchia) ancestors, although it is uncertain to which opisthobranch group they are most closely related. The pulmonates include a number of marine and freshwater families within several orders, but are predominantly terrestrial. By far the largest group of land pulmonates is the order Stylommatophora, but there are also several primitive families of slugs (Veronicellidae, Ra-thousiidae, and Onchidiidae) and snails (Ellobiidae), which are wholly or partly terrestrial. This entire group, excluding the ellobiids, is sometimes united as the Geophila, but it unclear whether it is monophyletic. Molecular studies show that the Stylommatophora are monophyletic, and may have evolved from a terrestrial ellobiid ancestor.
Classification within the Stylommatophora has traditionally been based on the morphology of the pallial system (which includes the lung, kidney, and ureter). Four primary groups, or suborders, were recognized: the Orthurethra, which were thought to be the most primitive, and from which the other three evolved; the Sigmurethra, which includes most of the stylommatophoran families; the Mesurethra, which is a small group with a reduced ureter; and the Heterurethra, which contains only the amphibious family Succineidae.
However, a recent molecular study by Wade, Mordan, and Clarke (2001) shows a very different pattern of phylogenetic relationships within the Stylommatophora. It suggests that there is a primary dichotomy between a smaller, "achatinoid" clade, which includes the "sigmurethran" families Acha-tinidae, Subulinidae, Freussaciidae and Streptaxidae, and a larger "nonachatinoid" clade, comprising all the remaining sigmurethran families, plus the Orthurethra, Heterurethra, and Mesurethra. The Orthurethra are shown to be a relatively advanced group equivalent to other large superfamilies. The
succineids (Heterurethra) are the sister group of a family of tropical slugs, the Athoracophoridae (together called the Elas-mognatha), and are also included within this larger "nonachatinoid" clade, as are the various families which comprised the Mesurethra. The various families of both slugs and predatory pulmonates are shown to have evolved independently numerous times.
There is no general agreement on the classification of terrestrial pulmonates, but that of Vaught (1989) represents a good recent compromise. Vaught's Stylommatophora contains 81 families arranged in 26 superfamilies. There are probably around 25,000 species worldwide. Additionally there are four families of "primitive" pulmonates with terrestrial representatives, which have relatively few species.
The four orders of Pulmonata, based on Burch 1982 and Jeffrey 2001, are the Stylommatophora (terrestrial snails and slugs), Basommatophora (mostly freshwater, also some terrestrial and marine snails and slugs); Systellommatophora (sluglike); and Actophila (marine, intertidal, and brackish-water snails).
The order Basommatophora (15 families, 50 or more genera, and at least 4,000 species) contains a number of relatively primitive families. The order as a whole inhabits a wide range of habitats. The majority of species are freshwater, but there are some terrestrial and intertidal marine families. Some of the better-known families include the Lymnaeidae, dextrally coiled pond snails, some of them amphibious, and some having limpetlike forms.
Members of the family Physidae, sinistrally coiled pond snails, commonly called tadpole snails or pouch snails, are widespread and can tolerate some pollution of their waters. The family Planorbidae, the wheel snails, orb snails or ramshorn snails, is the largest family, in terms of the number of genera and species, of freshwater pulmonates, and is found on all continents and most islands. Many Physidae species are intermediate hosts of the larvae of parasitic worms.
The order Systellommatophora (five families, 11 genera, 50 or more species) comprises sluglike animals with the anus located at the posterior end of the body, in contrast to the normal state of affairs for gastropods in having the anus close to the front of the body. Species of the family Onchidiidae have a posterior pulmonary sac, and those in the family Veronicellidae have discarded the pulmonate lung altogether and instead respirate through their skin.
The order Actophila (five families, nine or more genera, 25 or more species) comprises snails inhabiting salt marshes and mangrove stands. Most species are tropical. In most species, the inner shell is a single cavity, no longer compartmentalized.
The Stylommatophora conform to the typical pulmonate body plan. Their main diagnostic characters are the two pairs of retractile tentacles on the head. The upper, longer pair have eyes at the tips, and are concerned with sight and distant olfaction; the smaller, lower pair sense the immediate substrate and food, and are also used in trail following. Additionally, stylommatophorans have a long pedal gland which lies beneath a membrane on the floor of the visceral cavity, and an excretory system with a well-developed secondary ureter.
The shell encloses most of the body organs and is usually dextral (coiling clockwise), but is sinistral (anticlockwise) in a few groups; in some species both coiling directions are represented. The shell is normally cryptically colored, but may be brightly patterned in arboreal species. Some 16 stylom-matophoran families are slugs or semi-slugs, in which the shell has been drastically reduced or even lost entirely. In these groups the lung cavity also is greatly reduced and accessory respiratory structures such as the mantle folds are developed. The male and female systems open together as a single genital pore.
Among the primitive pulmonate groups with terrestrial representatives, the tropical veronicellid and rathousiid slugs have two pairs of tentacles, the upper pair with the eyes at the tips; the veronicellids have no lung. Onchidiid slugs, most of which are littoral, have a single pair of tentacles with eyes at the tips. All three of these families lack any form of shell. Ellobiids are snails possessing a single pair of cephalic tentacles, with eyes at the base. The genital openings of the male and female systems are separate in all four of these families.
The largest snails are the giant African land snails of the family Achatinidae, which have been recorded with a shell height of 8 in (20 cm), whereas the tiny European snail Punc-tumpygmaeum has an adult shell diameter of around 0.04-0.06 in (1-1.5 mm). The foot of the North American banana slug can reach a length of 10 in (25 cm) when crawling.
Pulmonates within the orders Basommatophora, Systel-lommatophora, and Actophila have diversified into an impressively wide range of forms, with an extensive and often odd variation of shell shapes and details of lung anatomy. There are species with dextrally and sinistrally coiled shells, planispiral shells, limpetlike forms with rounded or conical shells, and sluglike forms. All but the family Veronicellidae bear a functional lung derived from the mantle. The lung is a hollow space within the mantle cavity, lined with tissue liberally supplied with blood vessels for gas exchange. The lung communicates with the outside via a small passage and open-
ing called the pneumostome. The lung is rendered active by muscular movements within the mantle that alternately compress and expand the lung cavity. Some aquatic and marine families have evolved secondary gill-like structures within their lungs, while others have evolved gill-like organs on the outer body. Limpetlike forms have evolved from more snaillike ancestors several times within the Basommatophora.
Basommatophora bear a single pair of tentacles, the eyes placed at the bases of the tentacles. This category includes more primitive members of the subclass than the land snails or Stylommatophora. Some breathe air, others take oxygen from the water, and some are amphibious, either using a secondary gill when in the water or coming to the surface periodically to breathe.
Among the nonstylommatophorans, two rather primitive families, the Amphibolidae and the Glacidorbidae, still carry an operculum—a moveable, doorlike, chitinous lid that the animals use to close and protect the open end of the shell.
Land pulmonates occur in most parts of the globe, extending from hot deserts to beyond the Arctic Circle. They have found their way to even the most remote oceanic islands of the Atlantic and Indo-Pacific.
The nonstylommatophoran pulmonates have spread themselves geographically about as widely as the Stylommato-phora, including freshwater bodies and tropical to temperate intertidal zones, on all major landmasses and many islands.
Pulmonates occur in most terrestrial habitats, except for the extreme polar and desert regions, although the highest species diversity is found in the moist tropics. They typically live on or near the ground surface, although some families of slugs spend most of their lives burrowing in the soil, and many snails (and a few slugs) are arboreal.
Pulmonates outside the Stylommatophora inhabit tropical and temperate regions. Basommatophorans are mostly freshwater, living in ponds, lakes, streams, and rivers. Systellom-matophorans are terrestrial and intertidal-marine, and Actophila prefer tropical salt marshes and mangrove stands.
Other than during mating, there is little communication between land pulmonates. "Trail following" is used by some species in locating a mate, or in the case of mollusk-feeding predators, their prey. There is little evidence of territoriality, but crowding can induce aggressive behavior and cannibalism.
Pulmonates are hermaphrodites, and cross-fertilization resulting from reciprocal and simultaneous copulation is the norm. However, several groups are capable of self-fertilization. Sperm exchange can either be internal or external, and if the former, is often mediated by a spermatophore.
The daily activity pattern of most species can be described as crepuscular, the animals being active at dusk and dawn, with varying degrees of activity during the night. Weather is also an important factor, with moisture, but not heavy rainfall, inducing foraging even during the day. In dry conditions snails estivate, withdrawing into the shell and secreting an epiphragm to cover the shell aperture. Typical estivation sites are well above ground level, attached to shaded rock faces or on the stems of plants. During the winter many hibernate, buried in the soil or leaf litter. Homing behavior is quite well developed in some species.
As a whole, nonstylommatophorans lead slow, solitary existences foraging. A few species are carnivorous. Some freshwater pulmonates can regulate buoyancy—sinking, floating, and rising within the water by regulating the air content of the lung. Some can even navigate upside-down across the air-water surface.
Most pulmonates are herbivorous, living on fresh and/or dead plant material. Some species, especially arboreal ones, graze on algal films and have specially modified spadelike radular teeth. Slugs and snails also commonly feed on fungi. Several families of slugs and snails are predators, and are specialized for feeding on, for example, earthworms (testacellid slugs) or other snails (spiraxid snails). Most diurnal activity is concerned with foraging, and is crepuscular or nocturnal.
Many insect groups feed on snails and slugs: carabid beetles eat large numbers of slugs, and the larva of the glowworm Lampyris feeds almost exclusively on snails. Flatworms also attack slugs and snails. Birds may use a stone like an anvil to break open the snail's shell. Mammals, such as badgers, rats, and hedgehogs, amphibians, and some reptiles are also important predators.
The vast majority of nonstylommatophoran pulmonates leisurely graze on living and dead plant material, algal-bacterial film on intertidal rocks, and, in some cases, carrion. A few species are carnivorous, among them species of the fam ily Glacidorbidae (Basommatophora), snagging and consuming worms and other small aquatic or marine animal life.
Courtship is often elaborate in pulmonates and is known to last up to 36 hours in some slugs. It can involve the partners biting each other with their radulae, and the exchange of calcareous darts that pierce the skin and carry chemicals that stimulate sexual activity.
Most species lay eggs in batches in shallow cavities in the soil. Often these are calcified, either containing granules of calcium carbonate or having a calcareous shell. Most eggs are a just few millimeters in diameter, but the shelled eggs of Strophocheilus can reach a maximum diameter of 2 in (5 cm). The brooding of eggs by some Pacific endodontoid snails in the specially enlarged shell umbilicus is a form of maternal behavior, and some arboreal snails construct brood chambers of leaves in which the eggs are laid.
In representatives of several families, eggs are retained in the uterus until they hatch; true viviparity involving a form of placenta appears to be rare. The number of eggs laid varies enormously. Some species lay just one or two eggs each year, whereas the giant African land snail Achatina can lay several thousand in a lifetime. Incubation time varies with species and temperature, sometimes taking as little as three to four weeks, but extending to well over one year in the slug Testacella.
All species in the orders Basommatophora, Systellommato-phora, and Actophila are hermaphroditic. Individuals are capable of fertilizing or being fertilized, but only a few species are able to do so simultaneously, since in all but the exceptions, sperm and unfertilized eggs mature at different times. Most species can self-fertilize. Some species can reproduce parthenogenetically, laying unfertilized eggs that develop into adults. Species in the family Siphonaridae still retain a veliger larva during development.
Over 1,000 species of terrestrial pulmonates are listed by the IUCN, of which almost 200 are listed as Extinct, and a further 116 as Critically Endangered. These are mostly endemic snails in the Pacific Islands, where the main causes of extinction are the destruction of the native forest and the introduction of predators for biological control.
The IUCN also includes about 1,000 freshwater mollusks on the 2002 Red List. Problems besetting nonstylommato-phoran pulmonates include habitat destruction and pollution of freshwater bodies and intertidal marine areas.
Many slugs, and fewer species of snails, are major agricultural pests, attacking crops both above and below ground. They also act as the intermediate hosts of important nema-tode and fluke parasites of humans and domesticated animals. Helicellid land snails carry the fluke Dicrocoelium dendriticum, which infects cattle, and the giant African land snail harbors the larvae of the nematode Angiostrongylus cantonensis, which can cause meningitis in humans. Several of the larger species of snails are eaten as food.
Basommatophoran species, particularly in the family Physidae, are intermediate hosts for parasitic worms that go on to enter the systems of humans and domesticated animals. Some species are used as food by humans.
1. Great gray slug (Limax maximus); 2. Spanish slug (Arion lusitanicus); 3. Roman snail (Helix pomatia); 4. Rosy wolfsnail (Euglandina rosea); 5. Giant African land snail (Lissachatina fulica); 6. Agate snail (Achatinella mustelina); 7. Onchidium verruculatum; 8. Glacidorbis hedleyi; 9. New Zealand freshwater limpet (Latia neritoides). (Illustration by Patricia Ferrer)
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