Crystal Butterflies of the Sea

All chains of life in the open ocean are ultimately dependent on plankton. Photosynthetic micro-plankton convert the energy of sunlight into their own stores that are in turn commandered by animal plankton through consumption and digestion. Both animal and photosynthetic plankton provide food sources for larger animals, both plankton and nekton, and even deeper dwelling organisms may take their sustenance from the rain of planktonic corpses settling from above. A wide range of animal lineages may be identified among oceanic plankton, one of the most prominent being the gastropod group known as the Thecosomata.

An orthoconch thecosomatan, Clio pyramidata, copyright Russ Hopcroft.

The Thecosomata are small gastropods, rarely exceeding a couple of centimetres in size at their largest. Many marine molluscs will spend at least part of their lives as planktonic larvae but relatively few mollusc groups have taken the route that the Thecosomata have, remaining part of the plankton through their entire life cycle. They maintain their position in the plankton by means of broad expansions of the foot on either side of the mouth, known as parapodia. The appearance and movement of these parapodia have given the Thecosomata the vernacular name of 'sea butterflies'. They also inspired the name Pteropoda ('wing-foot'), used for a clade that unites the Thecosomata with another group of planktonic gastropods, the Gymnosomata. Historically, many authors have questioned the association of the pteropods, in part because of the differing dispositions of the parapodia in the two component groups (Gymnosomata, commonly known as 'sea angels', have the wings of the parapodia located further back on the body rather than around the mouth). Nevertheless, more recent studies have corroborated pteropod monophyly (Klussmann-Kolb & Dinapoli 2006). The Thecosomata themselves fall between two major sublineages, known as the Euthecosomata and Cymbulioidea (or Pseudothecosomata). Members of the Euthecosomata have well-divided parapodia and the viscera are contained within a delicate, translucent, calcareous shell. In some euthecosomes such as the genus Limacina, this shell is coiled like that of other gastropods, but in others the shell has become straight and bilaterally symmetrical, being conical or globular with lateral projections. Recent phylogenetic analysis suggests that the straight-shelled sea butterflies may form a single monophyletic lineage known as the Orthoconcha* (Corse et al. 2013). In the Cymbulioidea, the parapodia are fused around the front of the animal to form a single swimming plate. Of the three families of cymbulioids, the Peraclidae have a calcareous shell as in the euthecosomes. The Cymbuliidae shed the larval calcareous shell over the course of their development and replace it with a pseudoconch, a hardened gelatinous, slipper-shaped structure that is still secreted by the mantle. In the third family, the Desmopteridae, the shell has been lost entirely.

*In the early days of invertebrate palaeontology, pteropod affinities were suggested for a number of groups of early Palaeozoic conical shells of uncertain affinities, such as the hyoliths and tentaculitoids. It is worth noting that, at the time, the pteropods themselves were often thought to represent a distinct molluscan class independent of the gastropods. Such proposals have long since fallen by the wayside. Not only is there nothing to connect such Palaeozoic forms with modern pteropods but the most superficial of resemblances in overall shape to certain Orthoconcha, but all indications now are that the Orthoconcha themselves did not evolve until some time in the Cenozoic (Corse et al. 2013), leaving a gap of some hundreds of millions of years between them and their erstwhile forebears.

Cymbulia peronii, copyright Vincent Maran.

Live sea butterflies feed on a wide range of organisms, including both micro-algae and other planktonic animals. The ancestral radula is reduced or lost and prey is captured by means of a mucous web, globular in euthecosomes and a funnel-shaped sheet in cymbulioids (Gilmer & Harbison 1986). This web may be absolutely gigantic relative to the animal itself, reaching up to two meters in diameter. While the web is extended, the sea butterfly does not swim actively but hangs suspended in the water column below, drawing food into the mouth by means of tracts of cilia on lobes of the foot. A further mucous array may trail away from the animal containing faecal particles and/or particles rejected as food; this may keep such particles from re-entering the feeding web. Should the animal be disturbed, the mucous web is rapidly ingested or abandoned before swimming away. Sea butterflies have commonly been referred to as suspension feeders but Gilmer & Harbison (1986) noted that a case could potentially be made for considering them as predators. Though micro-algae make up a large proportion of thecosome gut contents, the mucous web allows them to also capture active prey such as copepods that might have otherwise eluded them. It is possible that such prey is in fact more important overall for satisfying the sea butterfly's nutritional requirements. A number of sea butterflies possess brightly coloured mantle appendages that may lure active prey; the faecal trails may also assist in this way.

Limacina helicina, copyright Russ Hopcroft.

Sadly, any discussion of Thecosomata is forced to end on a tragic note. Recent increases in atmospheric carbon dioxide have lead to oceanic waters becoming more acidic than previously, which in turn reduces the concentration of dissolved carbonate. Because carbonate is a vital component of molluscan shells, ocean acidification compromises shell production. Studies of recent thecosome samples show that their shells have become thinner and more porous as acidification increases (Roger et al. 2012). If this trend continues, we may reach a point where shell secretion becomes impossible for these animals, leading to tragic consequences both for the thecosomes themselves and for the countless other organisms ecologically dependent on them. In recent years, concern has been expressed that ecological degredation may mean that we can no longer see butterflies flying in our gardens; their marine analogues are no less vulnerable.

REFERENCES

Corse, E., J. Rampal, C. Cuoc, N. Pech, Y. Perez & A. Gilles. 2013. Phylogenetic analysis of Thecosomata Blainville, 1824 (holoplanktonic Opisthobranchia) using morphological and molecular data. PLoS One 8 (4): e59439.

Gilmer, R. W., & G. R. Harbison. 1986. Morphology and field behavior of pteropod molluscs: feeding methods in the families Cavoliniidae, Limacinidae and Peraclididae (Gastropoda: Thecosomata). Marine Biology 91: 47–57.

Klussmann-Kolb, A., & A. Dinapoli. 2006. Systematic position of the pelagic Thecosomata and Gymnosomata within Opisthobranchia (Mollusca, Gastropoda)—revival of the Pteropoda. Journal of Zoological Systematics and Evolutionary Research 44 (2): 118–129.

Roger, L. M., A. J. Richardson, A. D. McKinnon, B. Knott, R. Matear & C. Scadding. 2012. Comparison of the shell structure of two tropical Thecosomata (Creseis acicula and Diacavolinia longirostris) from 1963 to 2009: potential implications of declining aragonite saturation. ICES Journal of Marine Science 69 (3): 465–474.