Group Pteropoda
The common name pteropods at the order level and the scientific name Pteropoda are used for Thecosomata and Gymnosomata.
For anatomy and organisation see: Gymnosomata and Heteropoda in this stack.
Pteropods are common planktonic molluscs living in all marine environments, from the poles to the equator, from the surface to the bathypelagic depths. Most species are oceanic but many penetrate coastal waters; though real neritic representatives are not recognised. Pteropods are not the only pelagic molluscs. Besides the Cephalopoda, there are the pelagic prosobranchs, Heteropoda and several opisthobranch Nudibranchia, while in the Lamellibranchia one species, Planktomya henseni, is considered planktonic.
Pteropods were first described and illustrated by Brown in 1756. The first important monograph on the group was written by Boas (1886); he considered taxonomy, distribution and variation. Tesch (1913) published the second monograph that comprised almost all of the recent taxa from the large oceanographic expeditions. Boas (1886), Bonnevie (1913), Brazier (1878), Broch (1910), Dall (1885, 1908), Eydoux and Souleyet (1840, 1852), Gould (1861), Hedley (1903, 1911), Jeffreys (1877), Knipowitsch (1902, 1903), Meisenheimer (1903, 1903), d'Orbigny (1836 - 1846, 1853 - 1855), Pelseneer (1866, 1887, 1888, 1888, 1906), Quoy and Gaimard (1824 - 1826, 1832 - 1833), Schiemenz (1906, 1911) Sykes (1904, 1905), Tesch (1904, 1910), Vayssiére (1902, 1904) also published on the Pteropoda of the major oceanographic expeditions. Recently two monographs (Spoel, 1967, 1976) and a handbook (Lalli and Gilmer, 1989) summarised present knowledge on pelagic molluscs.
The pteropods are of special interest for ecological and geological studies (Biekart, 1989). The carnivorous Gymnosomata are usually solitary and do not contribute much to the zooplankton biomass except for some species in the polar seas. They show a high diversity in tropical waters and, as most species are specialised feeders, they take a special place in the tropical pelagic food web. The Thecosomata, the shelled species, are more abundant than the Gymnosomata and they evidently contribute to the carbonate cycle of the ocean. They leave a signal in the fossil record that can be important in studies on palaeoclimate, palaeoceanography and palaeocology (Buccheri, 1984; Diester-Haass, 1976; Herman and Rosenberg, 1969)
For studies on life history strategies and feeding behaviour (Lalli, 1972; Conover and Lalli, 1972, 1974; Richter, 1977; Gilmer and Harbison, 1986) the Thecosomata are especially interesting. Adaptations of their reproductive cycle to phytoplankton blooms are known and in one genus, Clio, asexual reproduction is recorded. In the Cavoliniidae and Pseudothecosomata mucus feeding is highly developed and many species use a unique kind of mucous web to collect food particles from surrounding waters (Gilmer, 1972, 1974). This feeding by mucous webs is also found in Euthecosomata.
Many pteropods can be used as indicators for hydrographic and climatic features (Hida, 1957; Chen, 1968; Chen and Hillman, 1970; Furnestin, 1978). In some cases species are used in others subspecies and ecological races can be used as indicators.
Studies on locomotion and buoyancy of pteropods are scarceÊ(Denton, 1964; Morton, 1964; Davenport and Bebbington, 1990; Mileikovsky, 1973). Recently attention has been given to the structures used in swimming (Fiege, 1990a and b).
Distribution
Pteropods are a geologically recent group. The oldest fossils are known from Miocene age. In all probability they originated from an Atlantic centre of speciation and this is still demonstrated in the distribution pattern of the mesopelagic genus Peraclis (Spoel and Heyman, 1986). Species of this genus have different ranges but all are found in the NE-Atlantic, off Dakar. It is evident that these deep living species do not reflect climatic influences and shallow water-masses; they probably preserved traces of an old pattern in their distribution. It is impossible to recognise climate influences in bathypelagic species such as Limacina helicoides; the fact that this bathypelagic species is restricted to the Atlantic Ocean and its deep water outflow may indicate that it originated in the oldest (late Cretaceous) deep-sea basin, the N-Atlantic Ocean. The bathypelagic species,Clio andreae,has a much wider distribution than the preceding species which can be explained by the occurrence of the juvenile stages at shallow depths.
In the species frequenting the epipelagic layers, influences of climate and climatic changes are visible but the direct effect of currents and water-masses is seen in their distribution patterns.
In studying pelagic distributions, one always has to distinguish between range, expatriation range and sterile expatriation range. The geographic area where the species reproduces is called the range; as reproduction is usually restricted to a special depth layer one can distinguish, in that range, a special breeding area or niche. Specimens are brought out of that range by currents and a fertile population can be found although it may not be able to support itself without immigration from outside of the range, this area is the expatriation range. When specimens are taken still further outside of the area, they may survive but lose their ability to reproduce and such areas are called the sterile expatriation range.
C. pyramidata is cosmopolitan and many forms are described which have a distribution along the climatic belts. There are representatives of the cold-temperate (pyramidata), of warm (lanceolata), of polar (sulcata) and subpolar (antarctica) waters. Related species, such as Clio convexa, also show latitudinal dispersal. Species that are restricted to water-masses such as Limacina lesueuri, do not occur in belts but are restricted to a special body of water. Limacina lesueuri is found in the Central water-mass of all oceans. As the species is easily expatriated to other warm waters, its pattern resembles a warm-water pattern. Diacria major is restricted more to one and the same water-mass, and does not shows strong expatriation as it is confined to the Central water-mass.
Diacria consists of both types of species and ranges and it can be used as a model for the overall biogeography of the group Pteropoda. There are two species groups in the genus, the 'quadridentata group' with 7 taxa and the 'trispinosa group with 9 taxa.
In the quadridentata group, D. danae 'subtropical' form, is the most wide spread, living in all oceans in the belts between 30°N-10°N and between 30°S-10°S. D. danae 'equatorial' form, is restricted to equatorial waters of all oceans; the pattern of this species and its forms are clearly found along the climate belts. D. quadridentata is an Indo-Pacific warm-water species that does not penetrate the Atlantic Ocean as the S African continent closes this basin off for strictly warm-water species. D. costata 'equatorial' form, living in the Indo-Pacific shows a range comparable to the preceding species although it is more narrow. In the Pacific it gives rise to a second form: D. costata 'central-water' form, this form is especially adapted to the Central water-masses. D. schmidti subsp. schmidti is restricted to the E-Pacific Ocean oxygen minimum area. This is a typical zoogeographic area with many endemic species. D. schmidti subsp. occidentalis is restricted to the W-Pacific coastal areas. D. erythra subsp. erythra is endemic to the Red Sea and NW Indian Ocean species; it probably originated in the Red Sea and later dispersed over part of the Indian Ocean. D. erythra subsp. crassa is endemic to the Red Sea.
In the trispinosa group the most wide spread species is D. trispinosa subsp. trispinosa which lives in all oceans between 40°N and 40°S in a broad climatic belt not interrupted by continents. D. trispinosa subsp. atlantica 'typical' form is a representative of the transitional waters of the N-Atlantic between 70°N and 40°N. D. trispinosa subsp. atlantica 'dark' form is found in the upwelling area off NW Africa and is especially adapted to this water-mass. Isolated populations of many other planktonic and nektonic groups are also found in upwelling areas. Diacria rampali lives in all oceans between 30°N and 30°S and obtains this broad distribution through contacts south of S. Africa by expatriation. Proof of this expatriation can be found in sedimented shells found south of Africa. D. maculata is found in the north western boundary currents of Atlantic and Pacific Oceans, it seems adapted to coastal water-masses with a tropical origin. D. piccola has so far only been collected from sediments so that there is no proof of a living populations. D. major occurs only in the Central-water-masses of all ocean, thus it is a typical water-mass linked species.
Vertical migration and distribution
Most pteropods show a more or less pronounced diurnal vertical migration; animals swim and feed at night near the surface and migrate at dawn and dusk so that they stay at greater depth during the daytime (Stubbings, 1938; Humphreys and Myers, 1968; Spoel, 1973; Kobayasi, 1974; Wormuth, 1981). In a few cases reverse migration, with shallow daytime occurrence is reported (Stubbings, 1938, Newman and Corey, 1984).
Each area has its specific hydrographic structure and most species are influenced by these conditions so that the day and night level differ from place to place. However, some species always migrate further than others; ie. Diacavolinia species migrate only over some ten metres while Clio pyramidata migrates over 100's to 1500 m daily (Spoel, 1973b).
Remarkable deviations from the normal diurnal vertical pattern can occur when the bottom topography is irregular. Above sea mounts deep-sea species may live at shallow depths and in very shallow waters neritic species may not find enough depth to migrate; they lay on the bottom as is sometimes found for Creseis acicula.
A recently discovered aberration from the normal vertical pattern can be induced by productivity and temperature deviations (Schalk and Spoel, 1988). When temperatures at greater depths are slightly higher than normal, bathypelagic species can occur in the epipelagic zone as discovered in the Banda Sea. When, in a certain area, productivity is above normal the diurnal vertical migration may be suppressed (Schalk, 1990).
Most species are epipelagic but typical mesopelagic species include: Clio recurva, Peraclis species and some gymnosomates such as Thliptodon and Cephalobrachia. Bathypelagic species include; the thecosomates Limacina helicoides, Clio chaptali, C. andreae and e.g. the gymnosomates Massya, and Schizobrachium. As mentioned C. andreae shows ontogenetic vertical migration; the juveniles being found higher in the water column than the adults. Ontogenetic migration is usually common in deep-sea species.
Ecology
It is apparent that the Thecosomata and Gymnosomata show completely different ecologies. The thecosomates are herbivorous, with a feeding system dependent on ciliary activity and mucus secretion. There is no feeding specialisation and besides diatoms, micro-zooplankton is also trapped in the mucous webs and consumed. Heteropods, fish, whales and gymnosomates are the main predators of thecosomates, although pelagic birds, sea turtles and medusae are also known to feed on Thecosomata.
The Gymnosomata predate mainly on Thecosomata. They are active hunters, seizing prey with complex organs beset with hooks, sticky glands and suckers. Few predators of gymnosomates are known; only Clione is known to be an important whale food. Parasitism in pteropods is described (StecheIs, 1907; Stock,1971, 1973; Stock and Spoel, 1976). Mainly parasitic copepods and trematodes infect these animals, while different species of hydromedusan ectoparasitic polyps are often found on the shells of Cavoliniidae (Steche,1907; Kramp, 1922; Rosen and Hamon, 1952; Michel,1985).
Shell bearing pteropods have an important role in the calcium-carbonate cycle. The aragonite shells accumulate calcium-carbonate, and thus bind CO2 from sea water and the atmosphere. Aragonite dissolves easily than calcite so that after death a large percentage of the pteropod shells are dissolved. Only when sedimentation occurs at shallow depths (<±1200 m depth, depending on the CCD level) are the shells preserved and calcium-carbonate is trapped in the sediment. The Persian Gulf, Red Sea and shallow areas of polar seas are known for their pteropod rich sediments.
Reproduction
Pteropods are protandric hermaphrodites and cross fertilisation is common but self fertilisation may occur. The whole life cycle is understood to take about one year in most species. The eggs are delivered in gelatinous ribbons or balls. A veliger larva hatches, metamorphoses and develops into a juvenile stage. For example in Cavolinia, Clio and Limacina helicina this simple type of reproduction occurs. In some species ovoviviparity is observed. In Limacina helicoides and Clio chaptalii ovoviviparity is explained as an adaptation to the deep-sea environment where protection of the young generation is crucial. Ovoviviparity also occurs in the epipelagic species Hydromyles globulosa and Limacina inflata.
Asexual reproduction is described for two species: Clio pyramidata and C. polita, but the reproductive cycle of these species is not completely understood. In both species schizogamy was observed; the adult specimen divides transversely in 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, stays in the shell and develops wings; with the wings completely developed this part also leaves the shell and starts a free swimming stage. Although, but this stage has not yet been observed, this part only has to deliver the eggs when the numerous ova in the body are fertilised with the sperm also present before schizogamy.
Development
Shell growth and development of the soft parts may occur simultaneously as in Limacina but they can also differ as in Cavoliniidae. The unequal development of soft parts and shell gives rise to skinny and minute stages. Some Pseudothecosomata have no shell but a pseudoconch develops. In Gymnosomata the shell development stops after the embryonic stage. So four different developmental strategies in pteropods can be distinguished, apart from the asexual reproduction type discussed above.
The development in Limacinidae, primitive Cavoliniidae and Peraclididae is the most molluscan-like. After the embryonic stage, thus after protoconch I, the juvenile produces protoconch II and the soft parts grow out regularly into the mature stage when the teleoconch is formed.
In Styliola, Clio and Cavolinia growth is normal to the end of the juvenile stage but then shell growth slows while the soft parts quickly elongate to reach their full length. When grown to full length, shell production starts again and the thin teleoconch is formed which contains an extremely small soft body, this is the minute or skinny stage. Not until the teleoconch reaches full size and shape the soft parts start to grow and finally reach maturity. Shell growth usually does not stop entirely but continues by very small increases of the aperture border and thickening of the shell.
In Hyalocylis, Cuvierininae and Cavoliniinae (except Cavolinia) the same development is found but in these species the shell actively breaks during the minute or skinny stage. The teleoconch is separated from the protoconch and its posterior end is closed by a septum, in Diacavolinia this is by fusion of the postero-dorsal and ventral shell sides into a joint. Only after loss of the juvenile shell parts the soft parts start to develop to maturity. The pteropod shell is composed of a more simple structure than the average gastropod shell, it is mainly composed of a single shell layer (Be et al., 1972).
In the Cymbuliidae there is no development of an adult shell after the juvenile stage (with left coiled shell) metamorphosis occurs and a pseudoconch is formed.
In the Gymnosomata the embryonic shell, formed in the egg, is lost and a typical juvenile naked stage is formed with three ciliated bands around the body. When animals grow older these ciliated bands are lost and gonads develop in the body. Only Paedoclione is an exception as the ciliated 'juvenile' normally shows sexual maturity; this genus is clearly neotenic.
Taxonomic trends
In the begin of this century descriptions of new species based on the typological species concept and morphological descriptions formed the hard core of taxonomy. However, Boas (1886) and Pfeffer (1880) first gave attention to the concept of variation. Many species were described as being represented by more than one subspecies or forma. With the theory of geographic speciation the geographic variation became very important (Spoel, 1967). In the late 1960's the cladistic and phylogenetic approach was stimulated by the theory of Hennig. In the marine environment isolation is a rare phenomenon as all water-masses tend to mix, isolated basins are absent and isolated subspecies are rarely found. Only the Mediterranean and Red Sea are slightly isolated and these may be areas where subspecies can develop.
Variation
In planktonic animals, with large distributional ranges over different climatic belts and ocean basins, variation is a common phenomenon. Species with a large north-south range tend to reflect the climatic influences while species occurring in different water-masses are usually morphologically distinct. Clio pyramidata shows clinal variation in shell shape, it is narrow pyramidal in the polar seas and broad lanceolate in the tropical waters; the embryonic shell also shows differences where the warmer the water the smaller the volume of protoconch I. This concerns two different trends of variation, the protoconch shows pure ecophenotypical variation dependent on temperature. The shell shape shows cline variation dependent on distinct selective pressure in the different water-masses of the range and geneflow between the populations. This geneflow smoothes out strong differences so that a gradual cline occurs. Interrupted geneflow gives stepped clines. In Clio steps in the cline are found at boundaries between major water-masses (Spoel, 1967).
Clio pyramidata thus can be used, not only as a hydrographic indicator species when different formae with different shell shapes are used, but also as an ecological indicator species for temperature when the embryonic shell dimensions are used (Furnestin, 1979). Diacria costata shows another typical example of water-mass variation (Leyen and Spoel,1982) in central waters the shells are smaller than in equatorial waters. More locally Diacria trispinosa from upwelling areas shows a different colour pattern from those found in the open ocean. In Cymbulia peroni size variation marks the difference between the Atlantic and Mediterranean populations (Furnestin, 1979). In Gymnosomata these relative small variations are less easily studied since the soft parts do not clearly show characteristic differences.
Phylogeny
Within the Gastropoda Limacinidae, Cavoliniidae, Peraclididae, Cymbuliidae, Pneumodermopsidae, Notobranchaeidae, Thliptodontinae, Cliopsidae, Clionidae, Hydromylidae, are monophyletic as concluded by apomorphies. Laginiopsidae cannot be considered as this family is poorly known. Based on the apomorphic character of the development of the hooks, the Gymnosomata, except for Hydromyles can be grouped together as a monophyletic group. These relations are given in the figure (Cladogram Gastropoda). For the Thecosomata a further clustering is problematic as real apomorphies are difficult to find for the entire group. They may be monophyletic but there is no real proof for this.
The Pteropoda are usually placed in the Opisthobranchia but it is very difficult to find an outgroup for them, the Gymnosomata were considered to be closely related 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 the eyes on top found in all pteropods, ornamented shells in Peraclididae, high spiral shells and fully developed operculum in Limacinidae and Peraclididae show that the pteropods still have close links to the Prosobranchia. The Pyramidellidae also form a group in between the Opisthobranchia and Prosobranchia. However, the Thecosomata may be polyphyletic and they are certainly not monophyletic with the Gymnosomata. The frequently proposed relationship of pteropods, especially thecosomatous pteropods, with the Bulloidae explained by their neotenic anatomy which resembles the bulloid larvae is not generally accepted (cf. Lalli and Gilmer,1989). Though there may be a few neotenic characters in the pteropods, there is no indication that pteropods, except for Paedoclione, are in any sense reproducing larval organisms.
Lalli and Gilmer see an indication for common ancestry of Thecosomata in the shared feeding behaviour and buoyancy strategy. Since the Thecosomata seem to have more characters in common with the Prosobranchia than with the Gymnosomata, the latter can be hypothetically be considered as more derived.
In the Opisthobranchia a high degree of parallelism is described and phylogenetic analyses are therefore difficult. The Pteropoda, as well as the Pyramidellidae and Philinoglossoidae, are evidently clades at the root of the Opisthobranchia and are still closely related to the Prosobranchia. The position of the Gymnosomata, closer to the Prosobranchia than the Thecosomata, is not in agreement with classical opinions. When the Vermetida, such as the Architectonicidae, are considered primitive shelled Euthyneura and both related to the Pyramidellidae (cf. Taylor and Sohl, 1962) it is interesting to note that feeding strategy in Vermetidae strongly resembles feeding behaviour in Thecosomata. In both groups food particles are collected by secreted mucous strings that are swallowed.
Thus somewhere in the ancient Prosobranchia there may have been an ancestor with mucus feeding, as well as, development of hooks and suckers in the buccal mass. This root may have given rise to Opisthobranchia, Pteropoda and some families 'intermediate' between the Prosobranchia and Opisthobranchia. A tentative cladogram showing these discussed relations is given in the illustrations (Cladogram Gastropod Phylogene).
The phylogenetic analysis shows the Euthecosomata (Cladogram Thecosomata) on a clade separate from the Pseudothecosomata, but both are monophyletic. Limacinidae are evidently ancestral to Cavoliniidae and Peraclididae are ancestral to the Cymbuliidae. The relation of Limacina and Peraclis is that of sister groups, they are not ancestral to each other.
The Clioninae are clearly monophyletic, however, the Thliptodontinae are not. The Cliopsidae and Pneumodermopsidae are related and derived families (Cladogram Gymnosomata).
An old idea that the Hyoliths from Cambrian and Ordovician times are related to Pteropods can be rejected on the basis of musculature (Dzik, 1978).
Promising results based on shell evolution published by Bandel et al (1984) showed a clear relationship between pteropods and Late Paleozoic primitive Prosobranchia Mesogastropoda are very promising.
Identification
It is difficult to provide a taxonomic key for the Pteropoda since comparable adaptations to floating behaviour developed during evolution of all groups of pelagic molluscs. However, we hope that the programme IdentifyIt (from the menu) will be a good tool, however.
Most species are small sized and a microscope is needed for identification and examination of the radula.
Techniques
Radula dissection: as indicated in the illustration, make a cross cut in the ventral side of the neck region and then pick out the oesophagus at the level of the ganglia. This section to the mouth is put on a slide and the tissues should be dissolved with KOH so that the chitinous plates become visible under the microscope.
Hooks and buccal cones (Dissecting buccal mass) can be made visible by making a cut in the hood over the buccal mass as indicted in the illustration.
Scuba diving also offers an unique way of collecting fragile pteropods. However, for quantitative purpose and for studying their biogeography other methods should be used. Collecting by plankton nets is the best methods, and when possible discrete depth nets which collect animals only from a fixed depth is preferred. In the past many collections were made with open nets and these samples offer a good opportunity to study the distribution of pteropods. Handling the nets needs special care since shelled and naked species are very fragile. Tows should be short in duration to prevent damage, the net should be gently opened and cleaned of its contents. Collecting Cymbuliidae needs very special care as the pseudoconchs are so loosely connected with the soft parts that they detach immediately. Neritic shelled species can also be collected from the beach by sorting the finer shell fractions.
When collecting with nets one should use different mesh sizes as the larger Gymnosomata and Cymbuliidae require a coarse meshed net while a small mesh is needed for the small Limacinids. The juveniles can best be collected with a foraminiferan net.
Fixation
Most shell-less species are best fixed directly in formalin, but narcotisation may produce better results. Alcohol is also a good preservative. Shelled species should always be fixed and preserved in alcohol 70% (acid free) as this does not dissolve the shell; formalin is never to be used for shelled species! Preservation in alcohol is advised since it is the best preservative for museum collections. When possible the labels should not go into the same jar as the animals as even a paper label may crush the shells. A scientific collection of pteropods, as for all plankton collections, should have the specimens labeled with locality, depth, date, time, water temperature and salinity.
Handling
The dry shells can be best handled with a wet brush, the specimens stick to it and can be transported. Fine flexible forceps can also be applied, eg. aluminum forceps also used by entomologists. A binocular microscope is needed to study most species and for the study of the buccal organs a stereo microscope is needed.
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