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RESEARCH NOTE AUTOTOMY OF THE POSTERIOR FOOT IN AGARONIA (CAENOGASTROPODA: OLIVIDAE) OCCURS IN ANIMALS THAT ARE FULLY WITHDRAWN INTO THEIR SHELLS Samantha D. Rupert1 and Winfried S. Peters1,2 1Department of Biology, Indiana/Purdue University Fort Wayne, 2101 East Coliseum Boulevard,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 species 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 Mollusca 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 genus 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 animal not yet completely withdrawn, aperture 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). 438 RESEARCH NOTE 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 Olivella 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.