Pteropoda
Introduction

Pteropods, an informal name for planktonic molluscs of the Orders Thecosomata (shelled pteropods) and Gymnosomata (naked pteropods), are common in all marine environments from the poles to the equator, and from the surface to bathypelagic depths. Pteropods are typically open-ocean organisms, and although many may be encountered in neritic waters, there are no real coastal species.

The first important monograph on the group, Boas (1886), concentrated on taxonomy, distribution and variability. Pteropoda of the major oceanographic expeditions were described in the following publications: Quoy and Gaimard (1824, 1832), d'Orbigny (1836-1846, 1841-1855), Eydoux and Souleyet (1840), Souleyet (1852b), Gould (1861), Pelseneer (1866, 1887, 1888a, b, 1906), Jeffreys (1877), Dall (1885, 1908), Knipowitsch (1902, 1903), Vayssière (1902, 1904), Hedley (1903), Sykes (1904, 1905), Tesch (1904, 1910), Meisenheimer (1905b, 1906), Schiemenz (1906), Broch (1910), and Bonnevie (1913). Starting with these results, Tesch (1913) produced a major monograph encompassing almost all recent taxa. Two recent monographs (van der Spoel, 1967, 1976) and a handbook (Lalli and Gilmer, 1989) summarize current knowledge of pelagic molluscs.

The Thecosomata comprise the shelled species (Limacina in oral view, Diacavolinia in ventral view, Cavolinia in ventral view, Cavoliniid lock system, Diacavolinia in lateral view, Cuvierina detached protoconch, Desmopterus in oral view, Cymbulia in oral view, Peraclis in oral view), of special interest for ecological and geological studies (Biekart, 1989). They contribute significantly to the carbonate cycle of the ocean, leaving a fossil record that can be important in palaeoclimatic, palaeoceanographic, and palaeocologic studies (Herman and Rosenberg, 1969; Diester-Haass, 1972; Buccheri and di Stefano, 1984). The Gymnosomata (Pneumodermopsis in ventral view, Clione in ventral view, Spongiobranchaea austr. radula, larval gymnosome ventral view), are shelled only in an early life stage, usually do not form swarms and do not contribute much to the zooplankton biomass except for some species in the polar seas. They are carnivorous and most species are specialized feeders.

Pteropods are protandric hermaphrodites and cross fertilization is the rule, although self fertilization probably also occurs. For most species the entire life cycle is presumed to take about one year. The eggs are delivered in gelatinous ribbons or spheres. A veliger larva hatches, metamorphoses, and develops into a juvenile stage. This simple scheme is valid for Cavolinia uncinata, Clio cuspidata and Limacina helicina, among others. Ovoviviparity is observed in some species. In Limacina helicoides and Clio chaptali this is thought to be an adaptation to the deep-sea environment, where protection of the young generation is crucial. However, the epipelagic species Hydromyles globulosa and Limacina inflata are also ovoviviparous.

Antarctic pteropods produce one generation per year. Subantarctic pteropods show different generation modes and seasonal differences in growth rates. For example, in the Southwestern Atlantic Limacina retroversa reproduces twice a year. One generation, born in early spring, shows high growth rates and precocious sexual maturation, and reproduces in late summer. The second generation grows during autumn but shows no growth at all during the winter, reproducing in the spring. This annual cycle matches the general primary production cycle of the Subantarctic zone, with two maxima, the main one in spring and a secondary one in early autumn (Dadon, 1989; Dadon and Lauría de Cidre, 1992).

Asexual reproduction has been described for two species: Clio pyramidata and C. polita, but the reproductive cycle of these species is not yet completely understood. Schizogamy was observed in both (van der Spoel, 1979): the adult specimen divides transversely at the middle so that an upper soft part with all the vegetative organs becomes detached and swims out of the shell. The lower half, with gonad tissues, remains in the shell and develops wings. Once these are functional, it also leaves the shell and starts a free swimming period. Probably this part delivers eggs only when the numerous ova in the body are fertilized with the sperm already present before schizogamy, but this has not yet been observed.

Development of the shell and the soft parts may be parallel (e.g., in Limacina), or may differ in speed, as in Cavoliniidae. Some Pseudothecosomata have no shell, developing only a pseudo-shell, and in the Gymnosomata shell development ceases after the embryonic stage. The development in Limacinidae, primitive Cavoliniidae, and Peraclididae is the most "typically molluscan". After the embryonic stage (i.e., after protoconch I is formed) the juvenile produces the protoconch II and the soft parts grow regularly to maturity, when the teleoconch is formed. Seasonal growth rates have been studied for Limacina retroversa in neritic waters. During the cold season the teleoconch shows little or no growth, whereas in spring growth rates are high (Dadon, 1989).

In Styliola, Clio, and Cavolinia growth proceeds normally to the end of the juvenile stage. Then shell growth continues while soft parts stop growing, only elongating to reach the shell rim. This produces a thin teleoconch which contains a very tiny soft body, known as the minute or skinny stage. Not until the teleoconch reaches full size and shape do the soft parts grow further to maturity. In adults shell growth usually does not stop entirely but continues very slowly at the aperture border, also involving some thickening of the shell.

In Hyalocylis, Cuvierininae and Cavoliniinae (except Cavolinia) development is the same, but the shell is actively broken during the minute or skinny stage. The teleoconch is separated from the protoconch and the junction is closed by a septum. In Diacavolinia this is accomplished by fusion of hind dorsal and ventral shell sides to form a joint. Maturation is reached only after loss of the juvenile shell parts.

In the Cymbuliidae shell development ceases after the juvenile stage (with left-coiled shell), and metamorphosis involves the production of a pseudoconch.

In Gymnosomata the embryonic shell, formed in the egg, is lost and a typical juvenile naked stage with three ciliated bands around the body emerges (larval gymnosome ventral view). With age these ciliated bands are lost and gonads develop. Paedoclione is an exception in that the ciliated juvenile normally shows sexual maturity, the genus thus being clearly neotenic.

Pteropod shell micro-structure is simpler than that of the average gastropod shell, being composed mainly of a single layer (Bé et al., 1972).

Gymnosomata are hunters, whereas Thecosomata are omnivorous mucus feeders. The solitary Gymnosomata are usually specialized feeders, the extreme example being that of Clione limacina that, in the North Atlantic, feeds only on Limacina helicina, and in the South Atlantic on L. helicina and L. retroversa (Conover and Lalli, 1972). Most other species are less specialized in their diet but all feed either exclusively or mainly on a few Thecosomata species (Lalli, 1972).

Thecosomata consume microplankton that is collected in a mucous trap (Gilmer, 1974; Gilmer and Harbison, 1986). All Pseudothecosomata produce free-floating mucus webs (Gilmer, 1972) of enormous size, with diameters 10 to 100 times that of the animal itself. The mucus with microplanktonic organisms adhering to it is eaten and a new web is produced. These webs have also been described for some Cavoliniidae. The existence of such webs is controversial in the Limacinidae, which also feed by means of a mucous apparatus. The mucus is secreted on the wing surface by glands. The food of Thecosomata consists chiefly of phytoplankton, including cocolithophorids, silicoflagellates, diatoms and dinoflagellates, and also foraminifers, radiolarians, and other protists.

The Limacinidae, Cavoliniidae, Peraclididae, Cymbuliidae, Pneumodermopsidae, Notobranchaeidae, Thliptodontinae, Cliopsidae, Clionidae, Hydromylidae, are all monophyletic as based on apomorphies. The evolutionary status of the Laginiopsidae, which have been studied much less, is unclear. Based on the apomorphic character of development of the hooks, the Gymnosomata, except for Hydromyles, can be grouped together as a monophyletic group. For the Thecosomata, in which real apomorphies are difficult to find, further grouping is problematic. They may be monophyletic, but there is still no real proof.

Pteropods are usually placed in the gastropod subclass Opisthobranchia. The Gymnosomata were considered to be close to the Anaspidae, and the Thecosomata close to the Pyramidellidae or Philinoglossoidae. The fully developed operculum in Limacina and Peraclis indicates that this classification of the Thecosomata may be questionable. The cylindrical tentacles with eyes on top in all pteropods, ornamented shells in Peraclididae, and high spiral shells with fully developed operculum in Limacinidae and Peraclididae, show that pteropods still have close links to the Prosobranchia. The Pyramidellidae also represent a group between the Opisthobranchia and the Prosobranchia.

The Thecosomata, however, may be polyphyletic, and are certainly not monophyletic with the Gymnosomata. The frequently proposed relation of pteropods (especially thecosomatous ones) with the Bulloidae by considering their anatomy neotenic (resembling bulloid larvae) is not generally accepted (cf. Lalli and Gilmer, 1989). Though there may be a few neotenic characters in pteropods, there is no indication that pteropods, except for Paedoclione, are in any sense reproductive larval organisms. Lalli and Gilmer (1989) suggest that the feeding behaviour and buoyancy strategy shared by all Thecosomata indicate their common ancestry. Inasmuch as the Thecosomata seem to have more characters in common with the Prosobranchia than do the Gymnosomata, the latter may be considered hypothetically more highly evolved.