Pelagic Molluscs

S. van der Spoel, L.J. Newman & K.W. Estep

Welcome to the Marine Species Identification Portal!
This site offers information on thousands of different species in the world's oceans and seas. The aim and
contents of this portal, as well as the latest updates, are treated in detail under about this site.

http://species-identification.org/species.php?
species_group=pelagic_molluscs&menuentry=groepen&id=5&tab=beschrijving

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 pelagicmolluscs. 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 pelagicmolluscs.
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 speciesare 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, 1990aand 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 breedingarea 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 Oceanoxygen minimum area. This is a typical zoogeographic area with
many endemic species. D. schmidti subsp. occidentalis is restricted to the W-Pacificcoastal 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 endemicto
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' formis 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 upwellingarea 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 currentsof 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 pyramidatamigrates 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 speciesmay 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 wingscompletely developed this part also leaves the shell and
starts a free swimming stage. Although, but this stage has not yet been observed, this partonly has to
deliver the eggs when the numerous ova in the body are fertilisedwith 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 growthusually 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 juvenilestage (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 gonadsdevelop 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
Seaare 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 speciesoccurring in different water-masses are
usually morphologically distinct. Cliopyramidata shows clinal variation in shell shape, it is narrow pyramidal
in the polar seas and broad lanceolate in the tropical waters; the embryonic shellalso 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 shellshape
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 specieswhen different formae with
different shell shapes are used, but also as an ecological indicator species for temperature when
the embryonic shelldimensions are used (Furnestin, 1979). Diacria costata shows another typicalexample of
water-mass variation (Leyen and Spoel,1982) in central waters the shells are smaller than
in equatorial waters. More locally Diacria trispinosafrom 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 Peraclisindicates 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.

[2 orders]
Taxonomic Picture Key