Pteropods (pteropod = 'wing-foot') are pelagic opisthobranch molluscs with wing-like extensions of the muscular foot (parapodia) that are used in swimming. They constitute quite a loose taxonomic grouping and are further divided into two other loose groupings: 1) the thecosomes or shelled pteropods, also called Sea-Butterflies and 2) the gymnosomes or Sea-Angels in which the adults lack shells.
In sea-butterflies the shell may be spiral, tusklike or fanlike and triangular or quadrangular in contour and encloses the whole animal (when it withdraws). The shells may bear spikes at their angles. The shell may be translucaent and gelatinous and secreted beneath the epidermis, what is known as a pseudoconch ('false shell') or an outer heavy calcareous shell (as in the euthecosomes or true thecosomes).
Flapping movements of the parapodia propel the animal. In the Sea-Angel Clione,the wing tips trace out horizontal figure-of-eights when maintaining vertical swimming. Swimming is necessary to maintain the vertical position in the water column as pteropods are denser than sea water and would otherwise sink. They can also swim horizontally and gymnosomes are particularly agile and can swim in a fast looping motion. Clione limacina can reach 85 mm in length (in the North Atlantic) but the maximum size decreases in more temperate waters. The wings can beat at up to 5 Hz (5 beats per second) in Clione and the animal may reach speeds of 5 to 10 cm/s.
In both groups, the rest of the muscular foot, which is used for creeping locomotion in many snails and slugs, is reduced to one pair of lateral lobes at the base of the wings on the ventral surface of the animal and one more posterior median lobe. The foot and wings of Sea Butterflies have been studied by Fiege (1990. Am. Mal. Bull. 8: 27-36). Both the wings and the foot lobes have a similar internal structure: a layer of striated muscle sits beneath the covering layer of epidermal cells whilst smooth muscle fibers form a series of internal struts bathed in haemolymph and connecting the ventral and dorsal surfaces of the structure. In the wings these struts can be clearly seen to form longitudinal rows along the length of the wing connected by horizontal branches of the muscle cells (at least in the thecosomes Creseis acicula and Clio pyramidata). A horizontal sheet of these smooth muscle cells divide the interior of the wing into ventral and dorsal chambers. Since striated muscles are required for rapid contractions of short duration whilst smooth muscles contract more slowly but in a sustained way, it has been suggested that the striated muscles generate the power for wing flapping, whilst the smooth muscle controls the shape and thickness of the wing, and hence also the internal hydrostatic pressure or rigidity of the wing. The rings can also be strongly retracted.
The naked pteropods, the sea-angels or gymnosomates, are carnivorous predators, hunting pelagic sea-snails. Some are equipped with sucker-bearing tentacles (reminiscent of those in cephalopods). In the pneumodermatid Sea-Angels suckered arms are brone on the ventral and ventrolateral walls of the buccal tube which is evertible. Clione lacks tentacles but has 3 pairs of buccal cones (cephaloconi) and one pair of hook sacs. The buccal cones are usually kept retracted inside the buccal cavity of the slit-like vertical mouth. When attacking potential prey the sea-angel puts on a fast burst of swimming, bending and looping and when striking the mouth opens widely and the buccal cones rapidly evert due to high internal hydrostatic pressure and seize the prey. These cones are covered in papillae and secrete sticky adhesive. (The papillae possibly act as the secretory outlets or these may be sensory.) If the sea-angel misses its target then the tentacles retract against almost immediately. This is called the 'fast-strike response' but sea-angels also have a second feeding mode called 'hunting' in which they 'aim blindly' by fast looping swimming with the buccal cones maintained in the everted position (Hermans and Satterlie, 1992. Biol. Bull. 182: 1-7). This hunting mode can be triggered by homogenised prey tissues introduced in the water (and is thus presumably triggered by chemoreception as the sea-angle smells or tastes the prey) and also by the presence of other sea-angels feeding nearby. The papillae on the cones occur in clusters of rosettes with 2 to 12 papillae per rosette.
The buccal cone and rosettes bear cilia. The hook sacs contain up to 60 tiny chitinous hooks in Clione limacina, arranged in 3 or 4 rough rows and these also evert with the cones and aid in prey capture and processing. Typical of opisthobranchs, pteropods feed by scraping with the evertible radula, a mobile belt-like plate lined by rows of hard chitinous teeth. In Clione limacina each row has a large central tooth and up to 12 erectile lateral teeth. the rows are continuously replaced as they wear down. In Clione antarctica the radula is reduced and each row has no central tooth and less than 8 lateral teeth on each side. The buccal cones are red-orange in colour in Clione and the yellow-orange digestive gland turns dark brown immediately after feeding. The posterior of the trunk contains a fluid-filled cavity.
The digestive system of Clione has been studied by Morton (1958. J. Mar. Bio. Ass. UK 37: 287-297). Salivary glands open beside the radula sac in Clione. The buccal cavity opens into the narrow oesophagus (which is pleated to allow expansion) and this opens into the large stomach-like digestive sac. From this a short intestine, with a ciliated lumen, runs anteriorly to the body wall to discharge small amounts of fecal matter through an anterior opening.
Sea-Butterflies secrete a sticky mucous web up to 6 cm across to catch food as they swim. Ciliary action withdraws the web in through the mouth. The foot lobes are ciliated and these cilia possibly help draw food and/or the web into the mouth. The wings are also frequently ciliated (on their ventral surface in Creseis acicula). In Cavolina inflexa the posterior half of each wing is covered with fields of cilia that drive currents in towards the mouth. The three foot lobes form ciliated ridges enclosing the mouth. It is thought that ciliary currents drive food in towards the mouth. To what extent Sea Butterflies feed by ciliary currents or by netting food with their mucous nets seems unclear. In some species the ciliary fields are reduced, for example occupying only part of the posterior of each wing in Creseis acicula and a single ciliated groove on the anterior wing margin, leading to the mouth, of Cymbula peronii.
Note the two lateral lobes of the foot beneath the head and between the wings; the median lobe is posterior of these (not shown). Clione is an important food for baleen whales as well as some commercially important fish.
The circulation is semi-closed, with some major vessels carrying haemolymph to and from the heart. the arteries empty into the haemocoel chambers of the body whilst the veins drain these chambers. Arteries supply the haemocoel of the wings and also supply some internal organs. In at least some pteropods, a diaphragm of connective tissue divides the body cavity (haemocoel) from that of the wings and foot. In the Sea Butterfly Cavolina there are valves within this diaphragm.
Detailed studies on the circulatory system of Clione limacina have been carried out by Arshavsky et al. (1990. J. Exp. Biol. 148: 461-475). Heart and wing actions appear to be under dual control: touching the head of the animal elicits an avoidance reflex in which the wings and heart stop and the animal sinks in the water column before resuming normal behaviour. Touching the tail elicits escape swimming in which both heart and wings accelerate. The heart also accelerates during periodic swimming bursts that last several seconds in normal activity. The heart consists of a single auricle which collects blood from a network of venous sinuses in the body wall (a sinus is an open cavity as opposed to a blood vessel which has an epithelial lining called the endothelium) and passes blood into the single ventricle which pumps blood through the aorta into a system of open-ended arteries. Blood exits the artery ends and enters the body cavity (haemocoel) where it becomes haemolymph before entering the venous sinuses to complete the circuit.
The heart is situated on the left inside the main trunk with the
visceral mass. It is regulated in a similar manner to the vertebrate
heart: it is myogenic, meaning that it can contract rhythmically without
nervous system inputs. It will also contract more forcefully when
stretched by an increased volume of blood returning to its chambers.
Motor nerves increase and decrease the frequency of heart contraction.
The left pedal ganglion sends one excitatory neuron to the heart and the
left abdominal ganglion sends three inhibitory neurons. (Abdominal
ganglion = visceroparietal ganglion = intestinal ganglion, see next
In Sea Angels eyes are generally found at the tips of the tentacles (anterior and/or posterior?). The Sea Angel Clione has two pairs of tentacles on its head. The mobile anterior pair are clearly visible in our model, but the posterior pair are very short and concealed inside pits on the back of the head. Clione has one pair of eyes but these are greatly reduced. Sea Butterflies have one pair of head tentacles with an eye on the tip of each. Generally, however, the eyes of pteropods are reduced, typically lacking a lens and having no visible pigment.
The central nervous system is quite well studied in Sea Angels. It consists of a collection of connected ganglia: one pair of cephalic ganglia innervate the body wall and appendages of the head; one pair of buccal ganglia innervate the foregut; one pair of pedal ganglia innervate the foot, wings and body wall; a pair of pleural ganglia and a pair of intestinal ganglia in the abdomen (abdominal or visceroparietal ganflia) innervates the viscera. Each pedal ganglion innervates the wing on teh same side of the body (ipsilateral innervation). The connectives between cerebral and buccal ganglia form a circumenteric ring encircling the foregut with the buccal ganglia below the gut and the cephalic ganglia above it. A pair of cerebrobuccal connectives are nerves connecting each cerebral ganglion to the buccal ganglion on the same side of the body. Each cerebral ganglion puts out one pair of cerebrotentacular connectives each of which ends in a small tentacular ganglion which innervates a tentacle. (Hence there are 4 tentacular ganglia, 2 pairs, for the anterior and posterior pairs of tentacles).
The neural circuit controlling swimming in Clione limacina by Arshavsky et al. (1985, Exp. Brain Res. 58: 263-272). Of about 400 neurons in the pedal ganglion about 60 exhibit rhythmic behaviour tuned to the swim cycle. One set of neurons activates the D-phase (dorsal flexion of the wings where the wings move backwards) and an antagonistic set activates the V-phase (ventral flexion or movement of the wings forwards). The circuitry is quite complex, but the diagram below illustrates the core of the circuit. (This simplified motif of an antagonistic control system could be a good system for students to model using network analysis / neural networks as an introductory exercise, for example in Java).
These two sets of neurons inhibit one-another when they are active (indicated by the 'pistols' or blunt-headed arrows in the diagram above). At least some of the connections between the neurons are electrical synapses (as opposed to chemical synapses) which electrically couple neurons together. When a group of neurons are connected by electrical synapses then activity in when of the neurons increases the likelihood that the others will activate simultaneously: electrical synapses synchronise neuronal activity. this is clearly important in correctly synchronisibng the activation of the swimming muscles. For example, N7 neurons are electrically coupled to N7 neurons in the contralateral ganglion (contralateral = on the opposite side of the body); N1 neurons are electrically coupled to N1 neurons in the same ganglion (ipsilateral, i.e. on the same side of the body).
Sea-Angels lack a mantle cavity (though sometimes the rudiment of a single gill remains) but large blood spaces under elevations in the body surface may serve a respiratory function as oxygen diffuses across the body wall. The shelled thecosomes, however, retain a mantle cavity which is usually ventral in position (dorsal in the spiral-shelled limacinoids = spiratellids) but this usually lacks gills. In Cavolina, however, there is a single very long crescent-shaped gill extending from the left side of the ventral mantle cavity to the roof on the right side of the mantle.
Pteropods are protandrous hermaphrodites, meaning that each individual develops first as a male then the female organs mature later. The penis of the pteropod is an evertible tube. In Clione it consists of vacuolated cartilaginous material and has a sucker-like structure behind its pointed tip. When retracted it sits within a sac-like sheath located in the base of the head. In shelled pteropods there may also be additional stylet-like structures that are used to stimulate copulation in the partner. Accessory copulatory organs, consisting of two leafy expansions attached to the foot by a stalk may occur and these are shed after copulation. Fertilisation is internal. The Sea Angel Hydromeles has an internal brood pouch to brood the fertilised eggs. this pouch degenerates and ruptures when the embryos have developed, releasing them into the haemocoel of the adult where it is presumed they escape by rupture of the body wall.
Typical of opisthobranchs, the egg undergoes spiral cleavage followed by gastrulation and hatches as a swimming veliger larva, swimming by means of the velum: a bilobed ciliated appendage. In Sea Angels, however, there is an additional postveliger larval stage, the polytroch larva, in which 3 ciliary girdles surround the body, giving it a segmented appearance. Some forms retain certain larval characteristics of the polytroch as adults (neoteny = retention of juvenile characteristics in the mature adult). For example, Paedoclione dolliformis is neotenic and is small, up to 2.5 mm in length with 3 ciliary bands: one around the posterior part of the head, one around the middle of the trunk and one around the tail. The two girdles on the trunk sit in annular troughs and hence divide the trunk up into 3 obvious sections. In Clione the posterior-most and sometimes the middle band remain as transparent bands in the adult, depending on species and geographical region. Clione antarctica retains traces of all three bands, the head band persisting as a ring of protuberances. In Clione limacina only traces of the posterior band sometimes remain (Gimer and Lalli, 1990. Am. Mal. Bull. 8: 67-75).