Crustacean Research 2018 Vol.47: 55–64 ©Carcinological Society of Japan. doi: 10.18353/crustacea.47.0_55 Transfer of the gatekeeper sea anemone Verrillactis sp. (Cnidaria: Actiniaria: Sagartiidae) between shells by the host hermit crab Dardanus deformis (H. Milne Edwards, 1836) (Decapoda: Anomura: Diogenidae) Akihiro Yoshikawa, Ryutaro Goto, Akira Asakura Abstract.̶ The symbiotic association between hermit crabs and sea anemones is a classic example of mutualism in the sea. Some species of hermit crabs have the ability to transfer the symbiotic anemones onto their new shells when they change shells. The hermit crab Dardanus deformis (H. Milne Edwards, 1836) (Decapoda: Diogenidae) carries some anemones on the dorsal surface of the shell (e.g, Calliactis) it inhabits and frequently has the sea anemone Verrillactis sp. (most probably conspecific with “Verrillactis paguri” in Uchida and Soyama, 2001) placed at the shell aperture. In this study, we observed that D. deformis transferred Verrillactis sp. from the aperture of its old shell to that of its new shell. This suggests that the peculiar position of Verrillactis sp. is determined by the hermit crab, which recognizes its proper position. Dardanus deformis engaged in a specific behavior of tapping before transferring Verrillactis sp. to the new shell. This is similar to the behavior shown previously by D. deformis to remove the sea anemones of Calliactis (Hormathiidae) from the dorsal surface of the shell. This suggests that this hermit crab species evolved a very similar tactile process for communication between the different Sagartiidae and Hormathiidae lineages of sea anemones. Key words: Symbiotic association, mutualism, behavior, marine invertebrate, quantitative observa- tion ■ Introduction and use of the sea anemones as emergency food (Imafuku et al., 2000). The symbiotic sea Many species of hermit crabs are known to anemones also benefit from their association carry symbiotic sea anemones on the external with hermit crabs in the form of access to food surfaces of the shells they inhabit or on their resources (Stachowitsch, 1979, 1980), ensured chelipeds (at least 41 species, 15 genera, 3 substratum availability (Conover, 1979; families of hermit crabs; at least 35 species, 14 Brooks, 1989), protection from predators, and genera, 7 families of sea anemones; Williams increased dispersal (Balss, 1924; Jonsson et al., & MacDermott, 2004; Antoniadou et al., 2001; McLean & Mariscal, 1973). These recip- 2013). The benefits for host hermit crabs in- rocal benefits have identified these relation- clude protection from predators, such as cepha- ships as “mutualism” (Antoniadou et al., 2013). lopods and fish, by the nematocysts of sea At least 24 hermit crab species have the abil- anemones (Ross, 1971; Balasch & Mengual, ity to transfer sea anemones to a new shell at 1973; Ross & Boletzky, 1979; McLean, 1983) shell change (Ross, 1974). Almost all the stud- Received: 1 Jan 2018. Accepted: 5 May 2018. Published online: 26 Jul 2018. 55 AKIHIRO YOSHIKAWA, RYUTARO GOTO, AKIRA ASAKURA Fig. 1. The symbiotic sea anemone Verrillactis sp. attached near the aperture of snail shells inhabited by the hermit crab Dardanus deformis (SL＝6.3 mm; female). (a), the original Neverita didyma hosoyai snail shell with Verrillactis sp. attached. (b), a Mancinella siro shell with Verrillactis sp. transferred from a Neverita didyma shell by the hermit crab (observation 1). (c), a N. didyma shell with Verrillactis sp. transferred from a M. siro shell (observation 2). (d), a Purpura panama shell with Verrillactis sp. transferred from a N. didyma shell (observation 3). (e), a N. didyma shell with Verrillactis sp. transferred from a P. panama shell (observation 4). (f), a N. didyma shell with Verrillactis sp. transferred from another N. didyma shell (observation 5). The scales indicate 5 mm. The white arrows indicate Verrillactis sp. 56 Crustacean Research 47 Crustacean Research 47 TRANSFER OF VERRILLACTIS SP. BETWEEN SHELLS BY HERMIT CRAB ies of the transfer have focused on sea anemo- ■ Material and Methods nes on the external surfaces of the host shells or on the hermit crab chelipeds (Ross, 1975). One D. deformis (shield length＝6.3 mm; fe- However, one interesting example, the sagartiid male) was collected from an intertidal rocky sea anemone Verrillactis sp. (most probably shore at Hatakejima Island, Shirahama, conspecific with “Verrillactis paguri” in Uchi- Nishimuro, Wakayama, Japan (33°41′46.6″N, da and Soyama, 2001) is attached to the colu- 135°21′48.0″E), on 6 September 2017 (Fig. mella (inner lip) of the aperture of the gastro- 1a). We brought it back to our laboratory, kept pod shell carried by the hermit crab (Fig. 1). it in a running-sea-water aquarium, and fed it Predators, such as fish, brachyuran crabs, and once every three days (e.g., krill and fish fil- octopuses (Reese, 1969), often attack the aper- lets). We observed the shell exchange and ture of the shell to eat the chelipeds and ambu- transfer of sea anemones by providing intact latory legs of hermit crabs, so this placement empty snail shells of similar size to the shell of Verrillactis sp. on the shell aperture, might that D. deformis had first used; these shells protect the crabs from predators like a gate- were obtained from a tidal flat at Shinjocho, keeper. Tanabe, Wakayama, and from a rocky shore No quantitative study has examined how a around Shirahama Aquarium, Kyoto University hermit crab transfers this gatekeeper sea anem- (33°41′33.3″N, 135°20′15.8″E). We provided, one, Verrillactis sp., when the crab changes its in an arbitrary order, these shells to D. deformis shell, but one old and anecdotal report is of in- and recorded its behavior with a video camera terest. Cowles (1920) observed that two Philip- (Panasonic, HC-V480MS, Japan). Time se- pine species of hermit crabs, Dardanus defor- quence analysis of the behavioral pattern was mis (H. Milne Edwards, 1836) (as Pagurus made based on the video recordings. The order deformis) and D. pedunculatus (Herbst, 1804) of the shells provided to the crab is shown in (as P. asper), carried two types of sea anemo- Table 1. The nomenclatures of the shell species nes (species not identified) on their shells: one followed the database of the World Register of large anemone on the top of the shell and an- Marine Species (WORMS), accessed on March other small one on the “underside near the pro- 9, 2018. truding head of the hermit crab” (i.e., at the Observation 1: the hermit crab initially car- shell aperture). Cowles (1920) reported that ried the shell of Neverita didyma hosoyai (Kira, these hermit crabs transferred each sea anemo- 1959), with two individuals of Verrillactis sp. ne to the same portion on the new shell when attached to the columella of the shell aperture. they changed their shells. Since these are dif- To promote a shell change, the outer lip of the ferent species the hermit crab must be able to shell was broken in a vise or with cutting pliers recognize the proper position of each sea to expose the chelipeds of the hermit crab, and anemone species on its shell. However, the a new intact shell of Mancinella siro (Kuroda, transfer of sea anemones onto the shell aper- 1931) was provided. The hermit crab changed ture has not been studied since Cowles’s obser- to the M. siro shell, and its behavior was ob- vations. served. The broken shell of Neverita didyma In the present study, we use both video re- (Röding, 1798) was removed from the aquari- cording and quantitative data to report in detail um. how the hermit crab D. deformis transfers Ver- Observation 2: the M. siro shell that now rillactis sp. to its new shell during a shell housed the crab was then damaged as above, change. and three new and intact gastropod shells, Cas- maria erinaceus (Linnaeus, 1758), Laevistrom- Crustacean Research 47 Crustacean Research 47 57 AKIHIRO YOSHIKAWA, RYUTARO GOTO, AKIRA ASAKURA Fig. 2. Observation 5: behavioral sequence of the hermit crab Dardanus deformis transferring the sea anemone Verrillactis sp. from a broken Neverita didyma shell to a new intact N. didyma shell. (a)–(c), the shell change behavior of the crab. (d), the first stage of the transfer: the crab began tapping the pedal disc and column of the sea anemone with its walking legs and chelipeds. (e) and (f), final stage: the crab used one or both of its chelipeds to pinch and remove Verrillactis sp. from the N. didyma shell (g) and (h), the crab placed Verrillactis sp. near the shell aperture using its walking legs and chelipeds. The black arrows indicate the position of Verrillactis sp. before, during, and after transfer. Table 1. The order of shell provided to the hermit crab. Observation 1 Observation 2 Observation 3 Observation 4 Observation 5 Before transfer Neverita didyma hosoyai Mancinella siro Neverita didyma Purpura panama Neverita didyma After transfer Mancinella siro Neverita didyma Purpura panama Neverita didyma Neverita didyma bus turturella (Kuroda, 1931), and N. didyma, After the observation, the vacant shells of M. were provided to the crab. The crab first chose siro, C. erinaceus, and L. turturella were re- the L. turturella shell and entered it, but imme- moved from the aquarium. diately exited and entered the N. didyma shell. Observation 3: the N. didyma shell that now 58 Crustacean Research 47 Crustacean Research 47 TRANSFER OF VERRILLACTIS SP. BETWEEN SHELLS BY HERMIT CRAB housed the crab was broken as described above provided. and an intact Purpura panama (Röding, 1798) The observations were made in daylight shell was provided. The crab changed from the hours on 7 Sept. (observation 1), 20:44 to N. didyma shell to the P. panama shell, and its 24:02 on 8 Sept.