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Influence of Proximal Stimuli on Swimming in the Sea Hare Aplysia Brasiliana

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Influence of Proximal Stimuli on Swimming in the Sea Hare Aplysia Brasiliana Journal of Experimental Marine Biology and Ecology 288 (2003) 223–237 www.elsevier.com/locate/jembe Influence of proximal stimuli on swimming in the sea hare Aplysia brasiliana Thomas H. Carefoota,*, Steven C. Penningsb a Department of Zoology, University of British Columbia, Vancouver, B.C., Canada b Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA Received 22 August 2002; received in revised form 20 November 2002; accepted 30 December 2002 Abstract Although the neurobiology and physiology of sea hares are extensively studied, comparatively little is known about their behaviour or ecology. Several species of sea hares swim, but the function of swimming is unclear. In this paper, we tested the hypotheses that swimming in Aplysia brasiliana serves to find food and mates, and to escape predators. Our data strongly support the hypothesis that swimming in A. brasiliana is related to feeding. Sea hares deprived of food overnight swam 12 times longer than ones that had been fed. When sea hares contacted food while swimming they invariably stopped, while those contacting a plastic algal mimic mostly continued to swim. Our experiments provided no evidence to support the hypothesis that swimming in sea hares is related to social behaviour. Sea hares deprived of copulatory mates for 3 days did not swim longer than ones held in copulating groups. Moreover, swimming sea hares never stopped swimming upon en- countering a conspecific. Our experiments also supported the hypothesis that swimming in sea hares is related to predation. Sea hares stimulated with a standardised tail pinch and exposed to ink of conspecifics swam four times longer than control individuals, and tail-pinched sea hares that released ink swam five times longer than ones that did not release ink. However, because predators of adult sea hares are mostly lacking and because sea hares often swim spontaneously without predators being present, we conclude that swimming behaviour in A. brasiliana is primarily related to food-finding. D 2003 Elsevier Science B.V. All rights reserved. Keywords: Sea hare; Aplysia brasiliana; Swimming * Corresponding author. E-mail address: [email protected] (T.H. Carefoot). 0022-0981/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0022-0981(03)00019-4 224 T.H. Carefoot, S.C. Pennings / J. Exp. Mar. Biol. Ecol. 288 (2003) 223–237 1. Introduction Marine gastropods of the genus Aplysia are among the best studied of all marine invertebrates. They serve as a model system for neurological studies (Kandel, 1979), and have provided natural-products chemists with a rich source of new compounds (Faulkner, 1992). Yet, in comparison with the extensive neurobiological and physiological literature on Aplysia, relatively little is known about their behavior and ecology (Carefoot, 1987). Here we focus on one notable aspect of behaviour, swimming. Of over 30 species of Aplysia, less than six are known to swim. Only two have been investigated in any detail, primarily from the standpoints of mechanism of propulsion, and duration, distance, and orientation during swimming. Neither the function of swimming nor the proximal cues to initiate swimming are well understood. Most of our knowledge of swimming in sea hares comes from the work of Hamilton and colleagues on Aplysia brasiliana in the northeastern Gulf of Mexico (Hamilton and Russell, 1982; Hamilton, 1986), and of Susswein and colleagues on Aplysia fasciata in the eastern Mediterranean Sea (Susswein et al., 1983, 1984; Ziv et al., 1991a,b, 1994). The two species appear to be closely related (Susswein et al., 1993; Medina et al., 2001). However, while both inhabit subtropical shallow marine waters, they differ in that A. brasiliana inhabits seagrass-bed habitats, favours red-algal food, and exhibits crepuscular/ nocturnal behaviour, while A. fasciata frequents sand and rock areas, eats mainly green- algal food, and shows principally nocturnal behaviour. Swimming bouts in both species are of short duration, averaging about 10 min, although occasional individuals may swim for more than an hour (Hamilton, 1986; Ziv et al., 1994). Swimming is more likely in calm conditions and, in A. brasiliana during swims in excess of 4 m distance, is more commonly at the surface and generally in an offshore duration (Hamilton and Ambrose, 1975; Hamilton and Russell, 1982). Theories on the mode of swimming in sea hares include sculling (Farmer, 1970; Bebbington and Hughes, 1973), jetting (Neu, 1932), and hydrodynamic lift (von der Porten et al., 1982). But where are the sea hares swimming to, and for what reason? Escape from predators, search for mates or food or more suitable habitat, and a mechanism for seasonal migration have all been proposed (Krakauer, 1969; Farmer, 1970; Aspey et al., 1977; Susswein et al., 1984; Hamilton, 1986). Predators are not unknown for Aplysia (Pennings, 1990; Rogers et al., 2000) but its repertoire of chemical defenses including purple ink, opaline secretion, and a wide spectrum of secondary metabolites in skin and digestive gland suggests that predation is unlikely to be a major influence on daily behaviour, especially for adults (reviewed in Carefoot, 1987). Likewise, while some laboratory swimming bouts of A. fasciata culminate in finding a mate, most do not (Susswein et al., 1984). Swimming in sea hares would most directly enhance reproduction if swimming individuals, on encounter, were to sink together to the bottom and commence copulation, but this has not been reported. A. fasciata, however, swims more when isolated than when in groups (Ziv et al., 1991a,b, 1994), and this behaviour could lead to aggregations and increased copulatory activity even if animals were not directly cued to stop swimming by the presence of conspecifics. Migration as part of the life cycle of sea hares has enjoyed past advocacy, but support for this idea has dwindled through lack of evidence (reviewed in Carefoot, 1987). T.H. Carefoot, S.C. Pennings / J. Exp. Mar. Biol. Ecol. 288 (2003) 223–237 225 The most likely hypothesis is that swimming behaviour is related to feeding. In support of this, Aspey et al. (1977) and Susswein et al. (1984) note that laboratory-swimming bouts of Aplysia will often terminate on encounter with food. Satiated A. fasciata (Susswein et al., 1984) and Aplysia pulmonica (Switzer-Dunlap, pers. comm.) also tend not to swim. Inhibition of swimming could be by feedback signals from stretch receptors in the crop, by post-ingestive nutritional cues, or simply by the increased mass of food in the crop. Here, we investigate the influence of several proximal stimuli on swimming in the sea hare A. brasiliana. Because food-finding seemed, a priori, to be the most likely explanation for swimming, and because feeding in sea hares occupies such a large portion of their daily time budgets (Susswein et al., 1983; Susswein, 1984; Carefoot, 1991a,b), we emphasised food-finding in the present study. Also included, however, were tests of mate-locating and predator-escape hypotheses. Questions we addressed included: (1) do fed sea hares swim less readily than food-deprived ones? (2) will swimming sea hares stop when food is encountered? (3) is a sea hare with a full crop- load of food too heavy to swim? (4) do recently mated sea hares swim less readily than ones deprived of mates? (5) will swimming sea hares stop on encounter with a potential mate? and, (6) does tail-pinching to mimic a predator’s attack enhance swimming? 2. Methods Adult-sized (200–300 g live mass) A. brasiliana were collected from harbour and breakwater regions at South Padre Island, Texas in May 2002 and maintained in 60-l plastic tubs at the Marine Science Institute, University of Texas. At this time of the year, the population was dominated by large adult animals, most of which were still vigorous and active. We did observe some senescent animals in the field, but none was collected. Where feeding on intact seaweeds was required, green alga Ulva fasciata and red algae, Hypnea musciformis and Gracilaria dibilis were provided ad libitum. Food-deprived sea hares were kept without food for a 24-h period prior to swimming tests. No individual was used more than once in an experiment. Some treatments required that the sea hares’ crops be force-filled via intubation (cf. Susswein and Kupfermann, 1975; Pennings and Carefoot, 1995). A short length of plastic tubing (4 mm o.d.) was gently inserted into the crop via the mouth after first touching a small bit of intact seaweed (Ulva) to the oral tentacles to initiate reflexive biting by the jaws and to enable passage of the tube past the radula. Once the tube was in place, a process requiring 3– 4 min, a 50-ml plastic syringe was attached and a selected volume of test material delivered over a 5-s period. The sea hares were unanaesthetised during force-feeding. Previous work on Aplysia spp. using intubation techniques (Susswein and Kupfermann, 1975; Pennings and Carefoot, 1995) showed that a volume equivalent to 10% of an individual’s live mass could be readily accommodated after it was deprived of food for 1 day. Assessment of blood- glucose levels following intubated deliveries of comparable volumes of seawater, agar, or cellulose in past studies of Aplysia dactylomela and Aplysia juliana indicated no significant stress-effects induced by this treatment or by concomitant handling (Carefoot, 1991a,b). 226 T.H. Carefoot, S.C. Pennings / J. Exp. Mar. Biol. Ecol. 288 (2003) 223–237 After an intubated meal, the sea hares were allowed to rest in individual 4-l plastic buckets for 1 h before being used in swimming trials. Swimming trials were conducted in an indoor circular fibreglass tank (0.5-m depth and 1.5-m diameter) containing non-agitated seawater at 24 jC, with release being just below the surface.
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