© 2001 by The Society for Integrative and Comparative Biology
Costs and Benefits of Opisthobranch Swimming and Neurobehavioral Mechanisms1
1 University of Washington, Friday Harbor Laboratories, 620 University Road, Friday Harbor, Washington 98250
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SYNOPSIS |
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After opisthobranch molluscs dislodge from the substrate during onset of swimming, the ensuing flexion or undulatory motions are usually not well oriented with respect to predators, prey or suitable substrate. Swimming motions are effective in launching animals off the substrate and elevating them into the water column where they are primarily transported passively by ambient waves and tidal currents. Both active swimming and passive transport on ambient currents may provide escape from predators, search for food and mates, and dispersal to new and potentially adaptive locations. However, loss of contact with the substrate and launching into the water column may also bring a high cost in terms of exposure to diverse risks. I illustrate several forms of opisthobranch swimming and describe their mechanisms and roles. In addition, adaptations of some opisthobranchs to reduce the risks of exposure to predators during swimming are suggested. These adaptations include small size, transparency or inconspicuous color to reduce predation while swimming, and neurobehavioral mechanisms of rheotaxis and geomagnetic sensitivity.
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INTRODUCTION |
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Although in general, gastropod molluscs are considered benthic dwellers, many, particularly opisthobranchs, are capable of coordinated swimming movements. Some (e.g., Clione limacina [Gymnosomata] and Limacina helicina [Thecosomata]) spend a large part of their lives suspended or swimming in the water column. Swimming is apparently an important adaptation in the opisthobranchs. It has evolved several times with different parts of the body adapted for muscular control of swimming movements, although as will be shown here, the muscles of the foot are always involved, even in species that swim by bending from side to side. The swimming movements themselves are also highly diverse in different species, with evolution of several fundamentally different kinds of cyclic undulatory motions.
Many opisthobranchs have unusual nervous systems by comparison with all other animals. Their relatively centralized nervous structures include what is recognizable as a brain or at least prominently cephalized ganglia in most species, and their brains or ganglia contain some of the largest nerve cells in the animal kingdom. These neurons, with diameters typically in the range 5–1,000 µm, are also often re-identifiable as individuals from animal to animal in the species, and even across species and larger taxonomic groups. Their respective neuronal identities are often resolvable by relative sizes, distinctive differential pigmentations and locations with respect to other prominent neurons, nerve trunks or ganglionic landmarks. Individual neurons may be identified morphologically and neurobiologists have also found many instances where neurons identified by morphological criteria are also apparently re-identifiable by their physiological function. Individual cells apparently often control similar interneuronal or motor functions from animal to animal, and again, structural and functional parallels often persist across larger taxonomic groups. Perhaps not surprisingly in these instances, the underlying neuronal circuitry, including synaptic relationships, electrical coupling, axonal pathways, dendritic arborizations and even neuronal capacities for in vitro reconstruction of neural circuitry, remain apparently closely linked to cellular identities established by morphological or physiological functions.
Not surprisingly, this combination of a cluster of interesting behaviors, with parallel evolution, and the capacity to identify individual neurons in central nervous system structures across species and higher taxa have attracted many workers with interests in behavior, and its underlying neural circuitry. There have been behavioral or cellular level physiological studies of swimming in Aplysia (Anaspidea), Clione and Limacina (Pteropoda), Dendronotus, Hexabranchus, Melibe and Tritonia (Nudibranchia). In several of these, the neurons responsible for generation of swimming behavior have been well studied, revealing specific roles for many of the neurons and some of the specific neuron-neuron synaptic or electrical pathways.
In general, however, less is known about the implications of swimming behaviors for the ecology of the animals that use them. In most instances there have not been field studies of the behavior of the animal to assess the adaptive value(s) underlying its evolutionary appearance in the species. Thus for instance the widely studied swimming behavior of Tritonia, elicited by brief contact with the tube feet of seastars like Pycnopodia helianthoides, is generally assumed to serve Tritonia as a protective function against predation. However there has never been a field demonstration that Pycnopodia actually preys on Tritonia, nor that swimming has any measurable protective value. Nor have studies been made to ascertain specific cost/benefits for swimming in these animals. Even less is known about the adaptive significance of swimming behavior in the several other species that swim.
In what follows, I review the swimming behaviors of several opisthobranchs, the adaptations of body form required, and generalities which emerge about the nervous system control. Additionally, since there are apparently serious risks and costs involved in swimming behavior, these will be discussed, along with the apparently protective behavioral and neural adaptations that have emerged in some species.
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SWIMMING BEHAVIORS OF OPISTHOBRANCHS |
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Although there are many more examples, seven species in the Orders Anaspidea, Gymnosomata, Thecosomata, and Nudibranchia are described that represent a wide range of swimming behaviors and include some unique and interesting mechanisms and underlying neural substrates.
All molluscs have internal organs (i.e., the visceral mass) surrounded by a body wall that is elaborated ventrally into a single, usually planar foot. The molluscan foot is often muscular, capable of contracting in all dimensions to form complex shapes, has a ciliated epithelium in many species and is usually primarily responsible for locomotion (Von den Porten, 1990
) Crawling is accomplished by gliding on a film of mucus, propelled by muscular waves, and/or by the beating motions of millions of cilia. Swimming is often driven by whole-body, dorsal-ventral, lateral, or combined twisting motions involving the musculature of the foot and body wall.
However another molluscan specialization is sometimes involved in swimming also. The parapodia can be viewed as a pair of wing-like elaborations of the foot that extends dorsally above the visceral mass. In some species the parapodia enclose a space containing the gills, and secretory organs responsible for chemical defenses (Reviewed in Johnson and Willows, 1999). Swimming in some species involves wing-like flapping of the parapodia (see contribution of Blankenship, [Yu et al., 2001]). A comparative look at the overall body forms and cross-sectional outlines of three opisthobranchs gives a sense of how the foot is elaborated to alter fundamentally the shape of the animal and also the mechanisms of swimming propulsion across the group.
In some opisthobranch species, e.g., dorids, in simplest terms, the body plan is pancake shaped, with foot surface down and dorsum up (Fig. 1). There may be a well-defined edge demarcating the portion of the foot that contacts the substrate, with a short foot extension lateral to that edge that extends to the boundary of the dorsum (Fig. 1A), forming a small cavity below the periphery of the dorsum. In other species, such as Tritonia, this foot extension from the edge of the foot contacting the substrate, to the boundary with the dorsum is more fully developed, and oriented more vertically, giving the animal distinct lateral surfaces, i.e., "sides." The cross sectional outline is a quadrilateral having a foot surface, a dorsum and two "sides." In other species, especially Dendronotids and Anaspids, the "sides" of the animal formed by this extension of the foot are even more fully elaborated making animals like Dendronotus, Melibe and Aplysia relatively tall and narrow. Sometimes the foot extends in this way even further to form the tall wing-like flaps (parapodia, as in Clione, Limacina and Aplysia) directed upward or laterally.
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Both the foot and the parapodia are innervated by nerve trunks originating most often from the pedal ganglia. Furthermore, most of the nerve cell bodies with axons projecting in these peripheral nerves originate in the pedal or (far less often) the pleural ganglia. Some of these neurons are unusually large and re-identifiable individually from animal to animal within a particular species and in some cases, even across opisthobranch taxa. Thus the pedal ganglia are usually a good place to look for most of the interneurons and all of the motor neurons innervating musculature responsible for swimming motions driven by contractions of muscle cells in the foot or parapodia.
Thus even swimming behavior that is driven by lateral flexions, or parapodial undulations (as in species shaped as in Fig. 1B and C) may be mostly driven by alternating contractions in muscles located in tissues that are foot or foot derived, on the "sides" of the animal. From this perspective, it is not unexpected that the evolution and variability across species of swimming mechanisms and the relevant neuron-neuron interactions may be mostly confined to neurons in the pedal ganglia which innervate foot tissue, and to a lesser extent the pleural ganglia (see other contributions to this symposium). Examples are seen in several groups. At least four species of the anaspid sea hare, Aplysia are reported to swim using parapodial waves. A well studied example, A. braziliana found in the West Atlantic, Gulf of Mexico and Caribbean coastal waters swims by generating dorsal-ventral waves that process from anterior to posterior along well developed parapodia with a repetition rate of about 0.5 Hz at 20°C (Farmer, 1970; Jahan-Parwar and Miller, 1978; Blankenship, [Yu et al., 2001]). The other three Aplysia species (described and compared by Bebbington and Hughes, 1973; Weevers, 1971) from European Atlantic waters, swim essentially similarly with posteriorad parapodial waves, but with parapodial waves that proceed at about 0.25 Hz.
The Orders Gymnosomata and Thecosomata (sometimes considered a single order Pteropoda) include many swimming species. Curiously, one of these swimmers the gymnosomate, Clione limacina hunts and eats one of the thecosomate shelled swimming species (Limacina helicina), and apparently little else. Both, however, swim by flapping for long periods (essentially their entire lives with brief pauses) wing-like extensions of the foot in sculling motions that are effective in maintaining directed, usually upward motion in the water column. Their swimming motions carry these extraordinary creatures on what are apparently diurnal vertical migrations. It is assumed, although not critically tested, that these migrations are adaptations for food capture and predator avoidance. It is also not critically known if long or short distance chemical, visual or other cues are used to guide swimming, whether as an adaptation to hunting or to escape.
Of the four major sub-orders of Nudibranchia, at least two (Dentronotidae, and Doridae) include examples of swimming species. The most spectacular of these is the dorid, Spanish Dancer, Hexabranchus. One of the four species of this sponge eating, brilliantly patterned, crimson animal is reported to reach over 40 cm in length on diverse Pacific tropical reefs (Edmunds, 1968; Farmer, 1970). The adaptive role of swimming is not known for this animal. It launches into the water column with a vigorous longitudinal ventral flexion, combined with anteriorad sinusoidal waves that pass continuously along the margin of the dorsum. The waves continue coupled to a series of dorsal and ventral flexions of the whole body. Swimming may continue for long periods, carrying the animal to the water-air interface, where it bobs near the surface. The animal is not commonly found exposed (to divers) on coral reef surfaces in daylight hours and is sometimes found hidden in coral crevices. Thus it may normally be crepuscular or nocturnal in its feeding and swimming behavior.
Its central nervous system is extraordinary. The pedal, pleural and cerebral ganglia are arranged as 3 bilaterally symmetric pairs on top of the buccal mass. The neuron cell bodies on the surfaces of these ganglia may be the largest (up to 1 mm dia.) and most distinctively pigmented (different cells—orange, yellow, white) of any in the animal kingdom. Unlike any others reported, many of these neurons protrude from the surfaces of the ganglia, each individual neuron encapsulated in the epineurial sheath. Nothing is known of the neurophysiological control of swimming behavior in Hexabranchus. This is due in part to the relative inaccessibility of the animal in tropical and remote locations, and its rarity at these sites. No effort has been made to culture Hexabranchus in the laboratory, a project whose success could be very helpful to progress of neurophysiological and behavioral studies. Hexabranchus is adapted to room temperature seawater, browses on sponge, and thus might make a suitable subject for the development of laboratory culture methods at higher latitudes.
The dendronotids show great variability in swimming mechanisms with some closely related species swimming exclusively by lateral flexions (e.g., Melibe leonina, and Dendronotus iris, and D. frondosus) and others (e.g., Tritonia diomedea) exclusively by dorsal-ventral flexions. Nonetheless, in all cases where the neuronal mechanisms have been studied, the motor neurons and most of the interneurons responsible for generation of the bilaterally coordinated side-to-side flexions are located in the pedal ganglia. Although one might have expected that bilaterally coordinated, side-to-side responses would involve more neurons and circuitry nearer the midline (viz., in the pleural or cerebral ganglia) the lateralized pedal ganglia are apparently the primary loci. The pedal and parapedal commissures may therefore be important by providing a direct route for the essential interactions, in addition to others through the midline ganglia and central commissure.
Benefits and costs of swimming
Opisthobranch swimming has not been studied in the field sufficiently to determine carefully its adaptive roles in any species. Nor have there been studies to indicate the relative costs of swimming. However some guesses emerge from observations of the kinds of stimuli that elicit the swimming response, the duration of swimming, field locations where is it observed to occur, and stimuli which terminate swimming (Table 1).
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In general, very little is known on all these issues. However it is clear that for those species that swim for long periods, all either are relatively small, translucent and colorless, (e.g., Clione, Limacina, Melibe) or if large, are opaque, brightly colored, and have contrasting patterning (e.g., A. braziliana, Hexabranchus). In some cases, e.g., a relatively visible species, that is potentially prey to diverse fish species, Clione antarctica has evolved a chemical defense system that strongly deters predation by fish (Bryan et al., 1995
). The coupling of these attributes suggests that there is adaptive value to protection against predation by being less visually apparent, chemically defended, or for larger animals, by aposematism.
Laboratory observations of swimming in Clione indicate that swimming may used for locating and capturing their Limacina prey (Norekian, personal communication; Lalli and Gilmer, 1989; Satterlie et al., 1985). This is primarily based upon the observations that both are pelagic swimmers most of their lives, and healthy specimens of Clione are rarely observed to stop swimming. When swimming stops for a few seconds, Clione sinks, and then starts swimming again. The only stimuli that reliably inhibit otherwise nearly constant, life-long swimming are reported to be parapodial or head contact with mechanical objects. When Clione makes close contact with its prey, it alters swimming direction and increases the rate to attempt to capture Limacina. Similar arguments could be made about swimming as a prey capture mechanism for Limacina.
Swimming in Melibe leonina occurs often spontaneously, and nearly always commences when the animal is dislodged from the substrate (normally blades of eelgrass, Zostera marina or from blades or stipes of kelp) and then it continues for long periods until the foot recontacts a substrate. However swimming may terminate for intervals spontaneously, and Melibe is sometimes observed drifting in mid-water in a non-swimming mode. Neurobiologists elicit swimming or terminate it abruptly, while recording in brain cells, by removing or replacing a piece of eelgrass from the foot of the suspended animal (contributions of Watson and Thompson to this symposium).
Hypotheses on these issues have been tested by field observations. For instance, Mills (1994) noted marked seasonality to observations of reproductively mature individuals of Melibe leonina carried by a combination of swimming and passive transport on tidal currents, and suggests swimming as a mechanism for reproductive dispersal. However the increased seasonal swimming frequency also corresponds with times when planktonic food is scarce suggesting that swimming may be an adaptation to the search for food. It is difficult to sort out and weigh the contributions of these and other adaptive possibilities.
Tritonia diomedea is rarely observed to swim in the field. In our work involving hundreds of hours of SCUBA diving observations of Tritonia, we have only seen a natural swimming response on one occasion, and on that occasion there was no apparent triggering stimulus for the response (unpublished observation). However it is very clear in the laboratory or in the field that vigorous swimming is invariably elicited by contact for a few seconds with one or a few tube feet from the large seastar, Pycnopodia helianthoides. This seastar is typically 0.5 m in diameter, relatively quick on its tube-feet (150 cm/min), and predatory on many molluscs, especially bivalves. Contact with Pycnopodia elicits escape behaviors in several bivalves, including scallops, and clams. Nonetheless, although we have often observed Pycnopodia co-occurring with Tritonia in the field, it has never been observed to chase or to capture the seaslug. In the laboratory the seastar has never been observed to capture and consume a healthy Tritonia. Thus, although Tritonia swimming is often assumed to be an escape response from predation, there is no direct evidence either in the field or in the laboratory to confirm it. This same swimming response can be elicited by contact with several other seastars, or by surfactants such as soaps and detergents, or by strong salt solutions.
Interestingly, Brown (1998) has shown that the Tritonia escape swimming sequence is powerfully inhibited by simply tapping its dorsum repeatedly. Tapping the dorsum for several seconds inhibits, the otherwise powerful and invariant response to seastar, salt or detergent contact, for hours. Other observations made in the field and laboratory suggest an explanation for this curious potent inhibition of swimming. Experiments by Lohmann and Willows (1987) and Lohmann et al. (1991) indicate that T. diomedea has a behavioral geomagnetic sense and that particular identified pedal ganglion neurons (Pd5,6) respond to changes in the ambient field by firing impulses. In a search for role(s) for geomagnetic orientation in the field behavior of the animal, using SCUBA we attempted to test the hypothesis that the geomagnetic sense was used to return to a ‘home’ location. We captured two populations of animals from deeper and shallower locations respectively, then exchanged them, placing each group on a line parallel to the shore. We returned 2 tidal cycles later at slack water to learn if the animals had respectively oriented back towards their original locations, i.e., did the animals on the deeper line orient primarily shoreward, and those on the shallower line orient primarily offshore?
Unexpectedly, we discovered that those on the shallower line had moved predominantly away from their ‘home’ location, i.e., towards shore, and those on the deeper line had disappeared entirely. This disappearance was despite a SCUBA search of an area larger than they would have been expected to be able to crawl in the 24-hr period. These results and further experiments confirmed (Willows, 1999) that the animals that were replaced on the shallower line, had exhibited a preferred shoreward orientation, rather than a "homing" preference, and that the animals on the offshore line had probably been carried away some distance in tidal currents. A series of experiments of this kind indicated that after disorientation, as occurs during the random tumbling involved in swimming Tritonia tends to orient along a magnetic heading that leads shoreward. Further, Tritonia persists in selecting the original shoreward heading, even if placed at a new site where the shoreward direction is reversed.
The original field experiment in which animals placed on a deeper line were not found again, suggested that it may be important for Tritonia not to lose contact with the substrate. Peak tidal currents are commonly 1–2 knots at Tritonia field sites, and tend to be stronger at greater depths. Apparently these disturbed animals recently replaced on the deeper line, were dislodged and carried off. After passive transport on tidal currents, these animals may have ended up relatively far from food and mates with few cues available to guide them back to prey and mates normally concentrated along the shoreline.
Early results (Willows, 1978) indicated that in a flume or Y-maze, when crawling, Tritonia orients strongly into the direction of oncoming currents. These experiments also showed that Tritonia crawls more rapidly when exposed to higher oncoming currents. Additional field and laboratory observations of responses to ambient flow conditions also suggest a well developed sensitivity to water current direction (Murray et al., 1992; Murray and Willows, 1996). Many neurons in the brain, especially pedal ganglion neurons, are keenly responsive to exposure to water currents. This work showed that Tritonia devotes a large part of its pedal ganglion neural circuitry to determining its orientation with respect to ambient water currents. Regardless of the actual location of food, mates, predators and other olfactory signals, the on-coming current brings with it sensory information that Tritonia may transduce and use, about food, mates, and predators. Tritonia can then orient towards or away from such cues by reference to the direction of the ambient currents, and thus its direction is an important frame of reference. Furthermore, current strength is also important because in addition to presenting higher resistance to be overcome by more rapid pedal locomotion (Willows, 1978), at very high levels it can dislodge animals and/or transport them great distances. The hazard presented by transport away from food and mates by strong currents is also presumably a factor while Tritonia is swimming. It is therefore interesting that animals carried away from their home location on a current would tend to return to that home location if, after swimming, and reattachment to the substrate, they crawl against the current at least for that half tidal cycle. Thus crawling in particular orientations to ambient currents is probably adaptive in the contexts of orientation to food, mates and predators, and to promote returning "home" following being carried away by tidal currents after swimming or loss of contact with the substrate for other reasons.
These and other experiments suggest that Tritonia may use both sensitivity to the geomagnetic field and rheotactic cues to avoid costs associated with swimming, viz., disorientation and dislocation offshore from food and mates. Movement in any other direction than shoreward in circumstances of disorientation would tend to take the animal away from food and mates, with evident maladaptive consequences. Interestingly also, Tritonia cannot crawl too far shoreward in its search for food and mates, because it will always encounter the shoreline as a barrier. On the other hand, it can crawl too far in any other direction and then move ever further from its prey and mates. Thus the shoreward direction may have a particular adaptive value when disorientation occurs.
Further unpublished observations in the field indicate that in unusually strong tidal currents, Tritonia actually builds (by pushing) a sediment berm ahead of itself, then stops crawling, and holds firmly to the substrate in the lee of the berm that it has built. This suggests an adaptation to avoid being dislodged and tumbled in the tidal currents in a way which could carry the animal away from its prey and mates. Thus one would expect swimming behavior to be inhibited at such times also, since swimming launches the animal into the water column where it may be transported great distances before resettlement. It may be that the original observation of Brown (1998) that mechanical pummeling of the dorsum inhibits swimming strongly, may be a manifestation of this same adaptive behavioral tendency to avoid swimming when there is danger of loss of contact with the substrate. This suggestion is made because it has been observed in the field and lab that the turbulence in the boundary layer near the water-substrate interface in medium or strong currents tend to pummel Tritonia's skin. One can observe directly that the skin ripples in such currents. This suggests at least, similar mechanical stimulation to the tapping mentioned above. Also, a similar kind of stimulation occurs when Tritonia tumbles along the substrate after dislodgment so that under these circumstances too, swimming would be inhibited. It is interesting that this tendency to hold onto the substrate apparently even takes priority over the option of escape by swimming even when Tritonia encounters a potential predator.
A final set of field observations confirms this tendency to avoid loss of contact with the substrate as occurs during swimming. As mentioned above, we observe in the field and laboratory that animals tend to orient directly into ambient water currents (Murray et al., 1996; Murray and Willows, 1996, 2000). Additionally, experiments in which the drag experienced by Tritonia as a function of its orientation to the current are revealing. Animals that are attached to the substrate and directed into currents produce about 1/2 the drag measured when orientation is at right angles to the current, and a smaller but significant reduction in drag by comparison with orientation opposed to the current. Thus, even the design of Tritonia's body shape is apparently adapted for avoidance of loss of contact with the substrate as occurs during swimming, especially if the animal is oriented into the oncoming current.
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CONCLUSION |
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The range of field and laboratory observations in several opisthobranch species described here suggests that swimming may have a high potential cost, as well as the benefits of food capture, dispersal, and escape from predators. The color, patterning, size, chemical defense, and transparency of several species suggest avoidance of predation may be a priority, and the development of rheotactic and geomagnetic senses, and body shape and behavioral tendencies to avoid creating drag in Tritonia all may be adaptations to avoid swimming or to recover orientation with respect to prey and potential mates after swimming.
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ACKNOWLEDGMENTS |
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I thank all my diving partners, Jim Beck, Glen Brown, Shaun Cain, David Duggins, Hana Jindrova, Ken Lohmann, Jim Murray, Nicole Phillips, Ion Popescu, Winsor Watson, Rebbie Williamson, and Michelle Woodbury for helping in many ways throughout this work. The projects described were supported by NIH Research Grant RO1 NS 22974 and I also thank the support staff of the University of Washington Friday Harbor Laboratories for invaluable professional help in all aspects of the work. The Symposium was supported by National Science Foundation grant IBN 9905990.
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FOOTNOTES |
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1 From the Symposium Swimming in Opisthobranch Mollusks: Contributions to Control of Motor Behavior presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: dwillows{at}u.washington.edu
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References |
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Bebbington, A., and G. M. Hughes. 1973. Locomotion in Aplysia. (Gastropoda, Opisthobranchia). Proc. Malac. Soc. Lond, 40:399-405.
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Edmunds, M. 1968. On the swimming and defensive response of Hexabranchus marginatus (Mollusca, Nudibranchia). Journ. Linn. Soc. (Zool.), 47:425-429.
Farmer, W. M. 1970. Swimming gastropods (Opisthobranchia and Prosobranchia). Veliger, 13:73-89.
Jahan-Parwar, B., and D. L. Miller. 1978. Central control of swimming in Aplysia braziliana. Biol. Bull, 153:446.
Lalli, C. M., and R. W. Gilmer. 1989. Pelagic snails: The biology of holoplanktonic gastropod mollusks. Stanford University Press, Stanford.
Lohmann, K. J., and A. O. D. Willows. 1987. Lunar-modulated geomagnetic orientation by a marine mollusk. Science, 235:331-334.
Lohmann, K., A. O. D. Willows, and R. Pinter. 1991. Identifiable molluscan neuron responds to changes in Earth-strength magnetic fields. J. Exp. Biol, 161:1-24.
Mills, C. E. 1994. Season swimming of sexually mature benthic opisthobranch molluscs (Melibe leonina and Gastropteron pacificum) may augment population dispersal. In W. H. Wilson Jr., S. A. Stricker, and G. L. Shinn (eds.), Reproduction and development of marine invertebrates. The Johns Hopkins University Press, Baltimore.
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Von den Porten, V. J. 1990. The functional morphology of the pedal musculature of the marine gastropods Busycon contrarium and Haliotis kamtschatkana. Veliger, 33:1-19.
Weevers, R. de G. 1971. A preparation of Aplysia fasciata for intrasomatic recording and stimulation of single neurones during locomotor movements. J. Exp. Biol, 54:659-676.
Willows, A. O. D. 1978. Physiology of feeding in Tritonia. I. Behavior and mechanics. Mar. Behav. Physiol, 5:115-135.
Yu, B., G. N. Gamkrelidze, P. J. Laurienti, and J. E. Blankenship. 2001. Serotonin directly increases a calcium current in swim motoneurons of Aplysia brasiliana. Amer. Zool, 41:1009-1025.[CrossRef]
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