Journal of The Malacological Society of London Molluscan Studies

Journal of Molluscan Studies (2011) 77: 437–440. doi:10.1093/mollus/eyr019 Advance Access publication date: 3 July 2011

RESEARCH NOTE AUTOTOMY OF THE POSTERIOR FOOT IN AGARONIA (: OLIVIDAE) OCCURS IN THAT ARE FULLY WITHDRAWN INTO THEIR SHELLS

Samantha D. Rupert1 and Winfried S. Peters1,2 1Department of Biology, Indiana/Purdue University Fort Wayne, 2101 East Coliseum Boulevard, Fort Wayne, IN 46805–1499, USA; and 2Goldring Marine Biology Station, Playa Grande, Santa Cruz, Guanacaste, Costa Rica

Correspondence: W.S. Peters; e-mail: [email protected]

Autotomy is the active shedding of a body part which occurs caraboides directed stabs to the head of the slugs and killed all of in a variety of emergency situations including attacks by preda- them (Pakarinen, 1994). Another generalist, P. melanarius,pre- tors (Stasek, 1967; McVean, 1975; Maginnis, 2006). The ferred certain slug over others (Foltan, 2004). Such pre- immediate advantage of autotomy – surviving an otherwise ference may establish an increased predation pressure that could deadly attack – comes at a price, which may include physical, favour the evolution and maintenance of costly defence mechan- energetic, behavioural and reproductive costs (Cooper, 2003; isms. Intriguingly, the preferred prey species were those capable Maginnis, 2006). While the evolutionary and ecological conse- of ‘tail’ autotomy (Foltan, 2004). quences of autotomy have been studied most thoroughly in The situation may be different in shelled gastropods, since lizards (Clause & Capaldi, 2006; Bateman & Fleming, 2009), autotomy does not seem to confer the same degree of life– the phenomenon also is known from numerous invertebrate saving benefit in species that can withdraw completely into a taxa, where it involves a wide variety of body structures protective shell as in those that cannot. Stasek (1967) compiled (Fleming, Muller & Bateman, 2007). In the autot- all cases known at the time and concluded that “prior to autot- omy occurs in bivalves, scaphopods, gastropods and cephalo- omy all these shelled gastropods have bodies too large to be pods; the older literature was summarized by Stasek (1967). entirely contained within the shell, while afterwards the shell Several additional cases have been reported more recently, completely covers the soft parts” (p. 9). Subsequent studies cor- mostly without detailed information on mechanisms and eco- roborated this conclusion and put it into an evolutionary logical implications (e.g. Warmke & Almodo´var, 1972; Hughes context. For example, in their review of the evolution of defence & Emerson, 1987). mechanisms in sacoglossan opisthobranchs, Marı´n & Ros (2004: In gastropods various body parts may be autotomized. In 232) stated: “When disturbed, species of the Lobiger cast nudibranchs autotomy of cerata (outgrowths of the body wall off their parapodia in a process known as autotomy, while that increase the body’s surface-to-volume ratio and facilitate species of the genus Oxynoe shed their tail since their shell has gas exchange) in response to attacks by predatory arthropods become reduced in size, allowing the head to be retracted but and the prey’s subsequent escape have been reported repeatedly not the tail or parapodia.” In the trochid Gena varia adeep (Bickell–Page, 1989; Piel, 1991; Miller & Byrne, 2000). transverse groove on the dorsal side of the foot marks an autot- Autotomy of the mantle margin has been observed in many omy zone (Fishelson & Kidron, 1968). Disturbed animals with- nudibranchs (reviewed by Stasek, 1967) and one prosobranch draw the head into the shell and attach strongly to the (Liu & Wang, 2002). Mantle autotomy generally appears to be substrate; the posterior part of the shell lies within the transverse a relatively slow process (Stasek, 1967) and no direct obser- groove in this situation. If the external force continues, the part vations of predator–induced mantle autotomy have been pub- of the foot posterior of the groove which cannot be withdrawn lished so far. The third category is the autotomy of parts of the into the shell will be autotomized. Fishelson & Kidron (1968: foot, usually the posterior portion (‘tail’), which has been 103) concluded that “this mechanism has been developed con- observed in all major groups of gastropods (Stasek, 1967). In ter- comitantly with the progressive reduction of the typical gastro- restrial shell–less slugs, ‘tail’ autotomy has been interpreted as a pod shell that occurs in this group of animals.” Thus, foot defensive response against predators that attack moving slugs autotomy in gastropods may have evolved in parallel with the from behind; the phenomenon seems restricted to fast–moving gradual loss of the protective shell, quite possibly because autot- species capable of escaping while the predator feeds on the auto- omy balanced to some degree the disadvantages incurred with tomized ‘tail’ (Hand & Ingram, 1950; Deyrup–Olsen, Martin shell reduction. To highlight the significance of Stasek’s (1967) & Paine, 1986; Pakarinen, 1994). In laboratory experiments compilation for the development of this idea and to obtain a with carnivorous carabid beetles, ‘tail’ autotomy helped to simple term for a complex evolutionary process, we will refer to reduce the predation rate when slugs encountered the generalist this notion as ‘Stasek’s scenario’. predator Pterostichus niger which attacked random body parts of On the Pacific coasts of tropical America – the Panamic its prey. In contrast, the specialist mollusc feeder Cychrus faunal province – several species of the genus Agaronia Gray,

# The Author 2011. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved RESEARCH NOTE

Figure 1. Foot morphology and autotomy in Agaronia propatula. A. Specimen showing a strongly pigmented autotomy line on the dorsal foot surface. B. Ventral view of same specimen as in A. C. Individual with light body pigmentation; the autotomy zone is indicated by a faint white line (highlighted by pointer line). D. When irritated, A. propatula withdraws completely into the shell. E. Rostral view of an not yet completely withdrawn, facing upwards. Abbreviations: do, dorsal surface of foot; ve, ventral surface of foot; asterisk, posterior tip of foot. The autotomy plane is marked by pigmented shallow grooves on the foot surfaces (pointer lines) and is oriented in parallel with the aperture. F. Specimen 25 min after autotomy; autotomized tissue placed next to the animal for comparison. G. Same specimen as in F, 17 days after autotomy with partly regenerated posterior foot. H. Animal with incompletely autotomized ‘tail’; the posterior foot is still connected to the animal through two lateral tissue bridges. I. Ventral view of an individual with bicoloured foot, perhaps indicating a previous autotomy event. Scale: shell lengths of animals shown are 32 mm (A, B), 34 mm (C), 33 mm (D), 39 mm (E), 33 mm (F, G), 27 mm (H) and 31 mm (I).

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1839 (Olividae) are common and abundant in the intertidal released it 17 days after the autotomy event. At that time, it zone of sandy beaches (Keen, 1971), where they prey mainly had regenerated about half of the autotomized posterior foot on semistriata Gray, 1839 of the same family as well as although it consistently ignored food. The coloration of the on various species of burrowing clams. Specialists on Panamic regenerated part differed strongly from the rest of the body gastropods have long known that “the posterior lobe of the foot (Fig. 1G). We made similar observations in four additional is easily broken off at a ‘tear’ line” in Agaronia species (Lo´pez, specimens which, however, could not be kept for more than Montoya & Lo´pez, 1988: 198), but no further details are avail- 24 h after autotomy. All of them actively explored the plastic able. Here we report field observations made in 2010 at two trays they were kept in and burrowed into sand if available, study sites located on dissipative sandy beaches several kilo- exactly as intact animals did. metres in length: Playa de Cuco, a public beach in eastern El The process of autotomy is not always complete. A small Salvador (138100N888060W) and Playa Grande in the Parque specimen was found in which the central part, about three Nacional Marino ‘Las Baulas’ in northwestern Costa Rica quarters, of the autotomy zone had separated the posterior (108200N, 858510W). foot from the rest, while lateral connections still remained At both sites, Agaronia species occurred at significant den- (Fig. 1H). The individual was kept in a seawater-filled plastic sities. On average, more than one actively hunting individual box for 36 h before it was released, but autotomy did not pro- per 10 m width of beach could be found on the sandy interti- gress during this period. The animal exhibited normal activity, dal at low tide. Agaronia species of the Panamic faunal province but could not withdraw the semi–autotomized posterior foot are morphologically variable and not easily distinguished, into the shell when irritated. particularly in the field. The identification guides available Freshly autotomized A. propatula or individuals showing (Keen, 1971; Lo´pez et al., 1988; Sterba, 2004) do not fully intermediate stages of foot regeneration were never observed agree on the taxonomic significance of various characters and foraging on the intertidal sandy plains of the study sites. the validity of species. Many of the specimens in the popu- However, 8% of the .600 specimens examined showed lations studied keyed out as A. propatula (Conrad, 1849) in the bicoloured feet in which the foot posterior of the autotomy line most detailed key available (Lo´pez et al., 1988), but a signifi- differed conspicuously from the rest (Fig. 1I). According to the cant proportion at each study site showed contradictory observation of the contrasting colour of a regenerating ‘tail’ combinations of characters and could not be identified unequi- (Fig. 1G), such bicoloured feet may indicate previous vocally. It is worth noting that no apparent behavioural autotomy and regeneration events. or ecological differences seem to correlate with these morpho- Possible predators of A. propatula that might be the targets of logical differences (unpubl.). In the following, we will refer to the autotomy response in the wild include birds, but we never our study subject as A. propatula, with hesitation. saw any of the waders, gulls and terns that foraged regularly Shells of A. propatula vary from very light grey to almost on the intertidal of our study sites feeding on Agaronia, black and from light orange to dark brown, with or without although this potential prey is easy to find when active. Snails speckles and spiral bands. The body is light grey to white, but submerged at high tide may be attacked by fish or crustaceans, may appear darker due to grey speckles that occur at varying but we have not observed this. On several occasions, we wit- densities (compare Fig. 1A and C). Some animals exhibit a nessed Agaronia specimens attacking each other. Unless the pronounced transverse black line on the ventral and dorsal animals differed significantly in size, such encounters ended surfaces of the metapodium (Fig. 1A, B). In others, this mark with the withdrawal of both opponents. However, if one indi- is of lighter grey tones, or even reduced to a faint white line vidual was significantly larger than the other, the smaller one (Fig. 1C). In any case, the posterior third of the metapodium was subdued and carried to a feeding position 5–10 cm under is separated from the anterior parts of the foot by a transverse the sand surface in the same manner as the standard prey plane that is marked by a ‘hoop’ of different pigmentation on O. semistriata (compare Supplementary material). Thus, foot the foot surface. This plane is an autotomy zone. autotomy may serve mainly in the defence against cannibalistic When irritated, A. propatula withdraws completely into its attacks in A. propatula, at least at our study sites. shell (Fig. 1D). In a late stage of withdrawal, the animals Authors of earlier studies (Stasek, 1967; Fishelson & Kidron, rotate their posterior foot clockwise (in dorsal view) by some 1968) concluded that the evolution of foot autotomy in gastro- 908 so that the left–right axis of the foot becomes oriented in pods might have been linked to the evolutionary reduction of parallel with the long axis of the elongate aperture (the shape the shell, and may even have been a factor balancing the nega- of the aperture is seen in Fig. 1D). Then, the posterior foot tive consequences of the loss of the protective shell. This rotates again by about 908, this time around the left–right hypothesis – ‘Stasek’s scenario’ – seemed perfectly plausible axis. The resulting geometry is shown in Figure 1E. The left based on the evidence available at the time, and may well margin of the foot faces forward while the right margin is explain the patterns of shell reduction and autotomy found in directed backwards; consequently, the ventral foot surface faces some taxa, for example, sacoglossan opisthobranchs (Marı´n& to the animal’s right and the dorsal one to the left. Most Ros, 2004). This does not imply, though, that Stasek’s scenario significantly, the autotomy plane now is parallel with the is the only context in which foot autotomy could evolve. Our apertural plane. As a result, the part of the foot posterior of observations establish A. propatula as an example for foot autot- the autotomy plane will form a plug in the aperture when omy in animals capable of withdrawing their bodies comple- retraction is complete. tely into their shells. A predator attacking an Agaronia will We first observed autotomy in A. propatula when we removed probably first trigger retraction; in the process, the autotomy moisture from a live specimen in preparation for weighing. plane in the Agaronia’s foot aligns with the plane of the shell Upon gently pressing a soft paper towel onto the tissue in the opening, and the posterior foot forms a plug in the shell aper- shell opening of the completely withdrawn animal, the ‘tail’ lit- ture (Fig. 1E). Predators incapable of swallowing the Agaronia erally fell out of the aperture. The sacrificed tissue weighed whole will then attack the prey’s soft tissue in the shell aper- 0.31 g, or 9% of the animal’s weight before autotomy. Placed ture, which is easily accessible since Agaronia species lack oper- in a seawater–filled plastic box, the animal re–emerged from cula. In this situation, autotomy will release the aperture plug its shell after 20 min and crawled about in a manner indistin- on which the predator has commenced to feed. It seems plaus- guishable from that of its intact conspecifics (Fig. 1F). Loss of ible that the predator will remain focused on the autotomized body fluids due to autotomy was not apparent. We were able tissue, providing the Agaronia with a chance to escape, at least to keep this individual until the end of our field trip and in a certain percentage of attacks.

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If our interpretation is correct, foot autotomy in Agaronia CLAUSE, A.R. & CAPALDI, E.A. 2006. Caudal autotomy and would seem to have evolved in the context of the loss of the regeneration in lizards. Journal of Experimental Zoology, – which is present or not in Olividae – and the 305A: 965–973. corresponding changes in the geometry of foot deformation COOPER, W.E. 2003. Shifted balance of risk and cost after autotomy that occur in the process of withdrawal into the shell. Several affects use of cover, escape, activity, and foraging in the keeled members of the operculum–bearing olivid genus Olivella ear–less lizard (Holbrookia propinqua). Behavioral Ecology and Swainson, 1831 withdraw their feet while folding them length- Sociobiology, 54: 179–187. wise (personal observations) rather than rotating them as DEYRUP-OLSEN, I., MARTIN, A.W. & PAINE, R.T. 1986. The Agaronia does (Fig. 1E), and autotomy has not been observed autotomy escape response of the terrestrial slug Prophysaon foliolatum (Pulmonata: Arionidae). Malacologia, 27: 307–311. in Olivella so far. The interpretation of the situation in this family is complicated by the fact that the anatomy of the nerve FISHELSON, L. & KIDRON, G. 1968. Experiments and observations on the histology and mechanism of autotomy and ring around the oesophagus “impedes an Oliva to really regeneration in Gena varia (Prosobranchia, Trochidae). Journal of swallow” prey of significant size (Marcus & Marcus, 1959: Experimental Zoology, 169: 93–106. 105). As a consequence, Oliva species secure their prey in a FLEMING, P.A., MULLER, D. & BATEMAN, P.W. 2007. Leave it pouch formed by the posterior foot while burrowing into the all behind: a taxonomic perspective of autotomy in invertebrates. substrate and feeding on their catch (Marcus & Marcus, 1959; Biological Reviews, 82: 481–510. Olsson & Crovo, 1968; Zeigler & Porreca, 1969: 11–14; Taylor FOLTAN, P. 2004. Influence of slug defence mechanisms on the prey & Glover, 2000; Kantor & Tursch, 2001). Since the posterior preferences of the carabid predator Pterostichus melanarius (Coleoptera: foot is critical for holding onto prey during feeding by “scrap- Carabidae). European Journal of Entomology, 101: 359–364. ing pieces off with the radula” (Marcus & Marcus, 1959: 105) HAND, C. & INGRAM, W.M. 1950. Natural history observations of or even for external digestion as suggested by Kantor & Prophysaon andersoni (J.G. Cooper), with special reference to Tursch (2001), it does not seem surprising that Oliva species amputation. Bulletin of the Southern California Academy of Sciences, have not been observed to autotomize their ‘tail’. However, 49: 15–28. Agaronia actually holds and transports its prey (preferentially HUGHES, R.N. & EMERSON, W.K. 1987. Anatomical and Olivella semistriata) in the same manner as Oliva species do (see taxonomic characteristics of Harpa and Morum (: Supplementary material) and still autotomizes its posterior Harpidae). The Veliger, 29: 349–358. foot. Thus, the standard behavioural prey-catching and KANTOR, Y. & TURSCH, B. 2001. The Oliva animal. In: Oliva feeding sequence is disrupted when autotomy occurs in shells. The genus Oliva and the species problem (B. Tursch & Agaronia. In connection with our observation of partial foot D. Greifeneder), pp. 75–102. L’Informatore Piceno, Ancona. regeneration over 17 days in an animal that refused food KEEN, A.M. 1971. Sea shells of tropical west America. Stanford (Fig. 1G), this suggests that the price an Agaronia pays for an University Press, Stanford, CA, USA. escape through autotomy may include the temporary loss of its LIU, L.L. & WANG, S.P. 2002. Histology and biochemical prey-catching capability. composition of the autotomy mantle of ficus (Mesogastropoda: We conclude that the family Olividae is a promising model ). Acta Zoologica, 83: 111–116. ´ ´ taxon for the study of the evolution of autotomy in biomecha- LOPEZ, A., MONTOYA, M. & LOPEZ, J. 1988. A review of the genus nic contexts that are quite distinct from Stasek’s scenario. Agaronia (Olividae) in the panamic province and the description of two new species from Nicaragua. Veliger, 30: 295–304. MCVEAN, A. 1975. Autotomy. Comparative Biochemistry and Physiology A, 51: 497–505. SUPPLEMENTARY MATERIAL MAGINNIS, T.L. 2006. The costs of autotomy and regeneration in Supplementary material is available at Journal of Molluscan animals: a review and framework for future research. Behavioral Studies online. Ecology, 17: 857–872. MARCUS, E. & MARCUS, E. 1959. Studies on Olividae. Boletim da Faculdade de Filosofia, Cieˆncias e Letras da Universidade de. Sa˜o Paulo(Zoologia), 22: 99–188. ACKNOWLEDGEMENTS MARI´N, A. & ROS, J. 2004. Chemical defenses in sacoglossan Support by Pilar Santidrian Tomillo and the staff of the opisthobranchs: taxonomic trends and evolutive implications. Goldring Marine Biology Station at Playa Grande, and Scientia Marina, 68 (Suppl. 1): 227–241. constructive comments by William E. Cooper Jr, Frank MILLER, J.A. & BYRNE, M. 2000. Ceratal autotomy and V. Paladino and D. Stefan Peters are gratefully acknowledged. regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators. Invertebrate Biology, 119: 167–176. Our field work was supported by an IPFW Undergraduate Summer Research Grant to S.D.R. In keeping with the senior OLSSON, A.A. & CROVO, L.E. 1968. Observations on aquarium specimens of Oliva sayana Ravenel. The Veliger, 11: 31–32 (plus 1 plate). author’s research permit for the National Park ‘Las Baulas’ (ACT–OR–D–015, Ministerio del Ambiente y Energia, Costa PAKARINEN, E. 1994. 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