Superfamily Atlantacea Philippi, 1853 (or Heteropoda)
The common name heteropods at the Superfamily level and the scientific name Heteropoda are used for the superfamily Atlantacea, composed of the families Atlantidae, Pterotrachaeidae and Carinariidae. Ponder and Waren (1988) considered this group as the Suborder Heteropoda, composed of one Superfamily Carinarioida
After the pteropods, the heteropods are the second most diverse group among the pelagic Gastropoda. Nature tried twice to provide the sea with swimming gastropods but was less successful with the heteropods as it is a group of visual predators. The need for light to aid in catching prey prevented these animals to adapt to deep and cold waters so that they are still restricted to the warmer shallow water, whereas pteropods developed adaptations to deep-sea and polar environments.
Heteropods may be of importance in the oceanic food web. The great diversity in the group is astonishing; some taxa share complex eye development with fishes and cephalopods, some share a gelatinous nature with jellyfish and there are exceptionally large sized species, usually not found in other molluscan groups, up to one metre long. Their general anatomy, behaviour and ecology, however, do not differ greatly among the taxa.
Most Heteropoda are found in oceanic areas but some, such as Oxygyrus keraudreni and a few Atlanta species, may penetrate deep into neritic waters. Distribution patterns of most heteropods show an avoidance to the centre of open oceans which gives them a distant neritic-like distributional pattern. In these waters they predate on small to medium sized prey such as small fish and fish larvae. Though some species may occur in large numbers they are of little economic value as they are restricted to the warmer waters with low economic fisheries value. The heteropods are not used for human consumption; they are eaten by fishes, turtles and birds. At one time the group was of commercial value. Before Linnaeus in 1766 described the first heteropod the shells of Carinariidae were a highly prized collectors item; individual shells were sold for hundreds of dollars each (Tesch, 1909).
The older literature from before 1888 is difficult to consult as synonymy problems are complicated, although very good studies on histology and anatomy of the heteropods were already published in these early years.
Benson (1835), Gegenbaur (1853, 1854, 1855), Gegenbaur et al (1853), Krohn (1860), Lesson (1827, 1830), Lesueur (1817), Niebuhr (1775), d'Orbigny, (1836-1846), Péron and Lesueur (1810), Philippi (1836), Souleyet (1852), and Troschel (1855) made valuable contributions to the study of Heteropoda and published both anatomical and taxonomic data. Smith (1888) made a major contribution in settling the nomenclature of the group. The more recent reports and revisions by Bonnevie (1920), Richer (1961, 1968, 1972, 1974, 1982, 1986, 1987, 1990), Taylor (1969), Taylor and Berner (1970), Tesch (1949), Thiriot-Quievreux (1973a), Spoel (1972, 1976) and Vayssiére (1903 1904, 1913, 1927) give a detailed taxonomy and biogeography for the group and the biology of the group is well described by Lalli and Gilmer (1989).
In terms of biomass, calcium-carbonate fixation or fisheries these molluscs are not of economic importance; for the study of pelagic life and gastropod adaptations the group is most interesting.
Distribution
Heteropod distribution is discussed by Aravindakshan (1977), Frontier (1973), González et al (1979), Magaldi (1977, 1984), Newman (1990), Okutani (1965), Sanchez (1984), Scarabino (1967), and Schiemenz (1911). The heteropods are found only between 40°S and 40°N in the warmer waters. The monotypic genera Oxygyrus and Protatlanta are found circum-globally at these latitudes. This is similar for Atlanta, except for the species Atlanta turriculata, Atlanta pacifica, Atlanta gibbosa, Atlanta tokiokai, Atlanta echinogyra, and Atlanta plana which are only known from the Indo-Pacific. Carinaria cristata, Carinaria cithara, Carinaria galea and Pterosoma planum are also restricted to the Indo-Pacific. Therefore 57% of the heteropods occur worldwide and 43% are restricted to the Indo-Pacific region.
The circum-global distributions do not show a continuous belt-shaped pattern as found in some pteropods. In Carinaria lamarcki a typical discontinuity in the Indian Ocean is found and an evident absence from the central Pacific Ocean. Any physical parameter explaining this pattern is obscure, although year round high temperatures (27°-28°) with small fluctuations seem to be avoided. Another pattern which is difficult to explain is found in Pterotrachea coronata where it is absent from the central Pacific Ocean and an unusual Atlantic-Indian Ocean pattern is found. A neritic influence can probably be detected, as well as avoidance of areas with very small annual temperature fluctuations. The same tendency is recorded for other heteropod species so that one may conclude that most heteropods show a distant neritic pattern combined with avoidance of areas with small annual temperature fluctuations.
The biotope of the group is restricted to the upper layers (0-500 m) of the ocean. The vertical distribution is described by Tanaka (1970, 1971). There is some doubt about the vertical migration in this group, evidently there is no strong diurnal vertical migration. Pafort-van Iersel (1985) concluded that there is little migration and that rather low temperatures can be endured by some species when they live at greater depths. The data given by this author indeed indicate some vertical shift during the 24 hour cycle but the species do not descend to great depths in complete darkness. As visual predators they avoid this area and have developed, as a camouflage, a transparent body and shell to escape from their own predators.
Richter (1968) stated that Pterotrachea scutata always lives below 100 m. As the number of specimens in the deeper hauls was usually low it is doubtful if there are species with populations normally living below 500 m.
Scattering layers composed of Carinaria cristata are described by Blackburn (1956) at 20 m.
Ecology
The ecology of Oxygyrus and Carinaria were best studied by Richter (1982) and Seapy (1980) respectively. Carinaria cristata forma japonica feeds on salps such as Doliolum and Thalia, some copepod species, Euphausia, other heteropods, Polychaeta, Hyperia, fish larvae, and medusae. A prey predator size relationship is found. Richter made an extensive study of the food web in which Oxygyrus is found. This genus, like all heteropods, is evidently carnivorous. The well developed eyes are used in locating prey. A very muscular proboscis and buccal mass, with a well developed radula, are used in capturing the relatively large prey. In most species the very large salivary glands probably have a special function in predation.
The animals swim with the ventral side and fin upwards and the dorsal side turned towards the depths. In slow swimming motion the ventral fin undulates; in quicker motion the whole body starts to undulate in an eel-like fashion.
Little is known about parasitism in heteropods, Lester and Newman (1986) described only rediae and cercariae from Heteropoda.
The eyes
The eyes are enclosed in an eye capsule to which the tentacle is attached. Two separate sensory nerves run to the eye and tentacle. The lens under the cornea is supported by a cup-shaped pigment zone. This pigment surrounding the eye has an opening (window) at the dorsal side so that, besides the light entering through the lens, light from underneath thus from the dorsal side, can also be observed. The light from the front produces a picture on the retina which is found at the bottom of the cup-shaped pigmented zone. The light from the dorsal side cannot give a picture but it is registered by the retina or by a secondary retina opposite the window as light intensity only.
The eye of Pterotrachea minuta is very cylindrical, the pigment zone shows a small U-shaped dorsal window. In Pterotrachea hippocampus the retina and lower part of the pigment zone are strongly broadened compared to Pterotrachea minuta. The eye muscles are indicated in this figure and it is clear that these can produce very complicated eye movements. The broadening of the eye base is also found in Atlanta helicinoides, Oxygyrus, and Cardiapoda. The illustration of the eye of Pterosoma planum clearly shows the dorsal window. The eyes can be useful in the identification of heteropods (Spoel, 1972).
Reproduction
Heteropods have separate sexes, minor sexual dimorphism is sometimes found in the tentacles, radula, fin sucker and in the absence or presence of a penis. Sperm transfer from male to female is accomplished with spermatophores. Sometimes spermatophore can be found attached to the shell of female atlantids. Females produce eggs in aggregated gelatinous egg masses that may be ribbon-shaped. Female Firoloidea are frequently seen with an egg ribbon still attached to the tail. The veliger larval stage develops a shell in all species; usually it is typically spiral in shape as in Atlanta or with low spiral as in Pterotrachea. In Oxygyrus keraudreni it is, however, completely planorboid. The veliger of heteropods have a velum with three or four pairs of lobes. A clear metamorphosis is found between larval and adult stage (Franc, 1949; Thieriot- Quievreux, 1969, 1971, 1975).
Phylogeny
The origin of the heteropods in the Mesogastropoda is obscure. A recent discussion can be found in Jamieson and Newman (1989) who indicated Littorinacea are most probably closely related but Naticacea, Rissoacea and other families are also to be found close relatives in literature. In all probability the group is monophyletic and at least of Eocene age. However, during the Early Eocene and Mid Miocene Atlanta and Carinaria fossils are already known (Lalli and Gilmer, 1989) so that all types must have developed during an earlier period. Although there is a clear trend in the adaptation to the pelagic life through all the genera, from Atlanta to Firoloidea, it could not be proven that all genera developed along one line, one clade. In all probability the Atlantidae, Carinariidae and Pterotracheidae developed separately from an ancestral group.
It is interesting to note that in Atlanta the 'original' clades all seem to represent Indo-Pacific endemic species so that the origin of the group seems to be in the Pacific or Indian Oceans.
Identification
The identification of the heteropods is sometimes difficult, especially since species of Atlanta are very difficult to distinguish. The papers by Richter listed in the bibliography are very useful in the identification of Atlanta. Special notes on identification problems are published by Tokioka (1955, 1961) who studied the operculum and whorl shape and by Spoel (1972) who used the soft parts for identification. The radula may be less useful but Richter stated that it is an important character.
The normal radula formula for Heteropoda is 2-1-1-1-2. The median tooth is unicuspoid or tricuspoid and has side wings on the basal plate. The central cusp may have denticulated sides. The lateral plates are uni-, di- or tricuspoid with a large outward projecting basal plate. The two additional teeth are unicuspoid, curved hook-shaped.
The operculum can be macro-oligogyral, micro-oligogyral or monogyral.
Techniques for the collecting
Seapy (1990) described the requirements needed for collecting heteropods and his main conclusion is that ten replicate net tows have to be made in order to get a correct idea of the populations of the most abundant species. The nets should have a large mouth area, 8 square metres mouth opening; a RMT (1+8) net proved to be adequate for collecting the larger species and a mesh size of 4.5 mm was used. To collect atlantid species a 0.5 mm or 0.32 mm mesh width is preferred, but to collect the juveniles one needs to use mesh sizes of about 0.1 mm. The optical stimulus of the net may result in net avoidance, so that the colour of the net should be adapted to the circumstances. As the shells and the shell-body connection are very fragile slow towing and short duration trawls produce better preserved specimens.
Fixation
Preservation and fixation are discussed in the chapter on pteropods and further information can be found in Spoel (1976). For handling heteropods it is advised to separate the shells that are best preserved dry from the soft parts that can go into alcohol (70%).
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