Kalinga ornata Alder & Hancock, 1864 (Nudibranchia: Polyceridae): a unique case of a sea slug feeding on echinoderms

The nudibranch family Polyceridae (Doridina) is subdivided into four subfamilies: Polycerinae, Triophinae, Nembrothinae and Kalinginae. Of these, Polycerinae, Triophinae and many Nembrothinae feed on bryozoans, while some Nembrothinae feed on other polycerids or tunicates (Mcdonald & Nybakken, 1997). However, there are no published data on the feeding habits of Kalinga ornataAlder & Hancock, 1864, the single species of Kalinginae. Kalinga ornata has been recorded throughout the Indo-West Pacific (Rudman, 1999; Gosliner, Behrens & Valdes, 2008) and grows to 200 mm (Alder & Hancock, 1864). The present study is the first to demonstrate that K. ornata feeds on ophiuroids, based on field observations and faecal analysis. Four individuals of K. ornata were collected among floating seaweed at 1 m depth on the rocky shore at Myogane-misaki Cape, Chiba, Japan (35°9′N, 139°48′E) on 23 August 2009. Specimens were maintained in an aquarium without food for 5 days. Then, several benthic animals that were commonly found at the collection site were put into the aquarium and we fortuitously discovered that K. ornata ate ophiuroids. Field experiments were carried out on 3, 5, 28 and 29 September 2009. All four animals were transferred from the aquarium to an area of sandy sea bottom with scattered rocks (6–7 m depth) at the collection site and confined in a plastic cage. Approximately 2 h after acclimation to ambient conditions (23–24°C) the specimens of K. ornata were released from the cage and given over 20 prey items in succession, including several ophiuroid species, placed 5 cm ahead of the crawling K. ornata. Several prey items that were not eaten by K. ornata individual No. 1 were subsequently given to individual No. 2. After each field experiment the sea slugs were returned to the aquarium and fed once or twice a week with ophiuroids (e.g. Ophiothrix exigua) until the end of the field experiments. The results of the feeding trials in the field are given in Table 1. When K. ornata encountered prey items, different responses were shown depending on the prey. The observed behaviours were classified into four categories: (A) Ignored: no apparent reaction; (B) Touching: prey touched with oral tentacles, but ultimately ignored (Fig. 1A); (C) Swallowing whole: as soon as oral veil tentacles touched the prey the buccal apparatus was everted to capture it (Fig. 1B); (D) Swallowing in pieces: arms of the ophiuroid bitten off from the disk and swallowed, and disk sometimes swallowed subsequently. Results of field experiment using Kalinga ornata and their preys. *See text for details of each behaviour. †NR, no record. ‡Diameter including spines. §Major radius. ¶Diameter of disk. #Ophiothrix sp. 1 is probably Ophiothrix exigua or O. ciliaris. Results of field experiment using Kalinga ornata and their preys. *See text for details of each behaviour. †NR, no record. ‡Diameter including spines. §Major radius. ¶Diameter of disk. #Ophiothrix sp. 1 is probably Ophiothrix exigua or O. ciliaris. Kalinga ornata. A. Individual No. 1 touching Holothuria cf. moebii with the oral veil tentacles; it did not subsequently feed. B. Individual No. 1 feeding on Ophiothrix sp. (Photo by Hisao Takeuchi). C. Individual No. 1 buried in sand. D. Individual No. 2 huddled into a sphere and floating up to just below the surface. For length of specimens of K. ornata, see Table 1. All four K. ornata ate only ophiuroids in the field experiments and consumed several ophiuroid species (Table 1). Other organisms, such as algae, nemerteans, bryozoans, other sea slugs, polychaetans and crustaceans, were usually ignored. The sea slugs touched some nonophiuroid echinoderms with their oral tentacles, but never ate them. The predators rarely failed to capture the ophiuroids, even if the prey struggled to escape. When K. ornata bit off part of the arm of its prey, it usually caught and ate the remaining portion later. In general, ophiuroids readily autotomize their arms when disturbed, but autotomy was not observed in these experiments. The mode of predation of K. ornata is similar to that of Gymnodoris rubropapulosa (Bergh, 1905) (Doridina: Gymnodorididae), which feeds on other nudibranch species. While G. rubropapulosa usually swallows prey whole, when the prey is too large it bites off only a portion of the prey (Nakano & Hirose, 2011). Similarly, K. ornata appears to change its mode of feeding depending on prey size and/or species. The faeces egested from the Chiba specimens after the field experiments were examined under a light microscope. Ossicles of ophiuroids, mainly those from the arms and arm spines, were found. Our results suggest a strong dietary preference of K. ornata for ophiuroids. Kalinga ornata is so far the only nudibranch known to feed upon ophiuroids. Few other organisms eat ophiuroids and therefore there may be little competition for this food resource (e.g. Cattaneo-Vietti, Burlando & Senes, 1993; Fujita, 1996; Battle & Nybakken, 1998; Ganmanee et al., 2003; Ohmura, Hamatsu & Takahashi, 2005). During the daytime field experiments individual No. 1 was twice observed to burrow into the sand, taking 19–23 min to bury itself completely except for the gill (Fig. 1C). Individual No. 2 once huddled up into a sphere by folding its foot and floated upwards (Fig. 1D); when we brought it back to the sea bottom it crawled and burrowed into the sand, taking 20 min to bury. There were no prey items in the sand, suggesting that burrowing behaviour is not for foraging. At another locality K. ornata has been observed buried in this same manner during the day and moving across a rocky area at night (3–10 animals observed at Kagoshima, Japan, in 1.5–4 m depth; S. Dewa, personal communication). We thank Ms Akemi Suzuki and Mr Hisao Takeuchi for generous help with the field experiment in Chiba and providing the photograph. We also thank Genya Okano, Masami Uno, Shin-ichi Dewa, Yuki Miyaoka and Dr Toshifumi Wada (Coastal Branch of Tottori Prefectural Museum) for providing information about K. ornata. We are also indebted to Dr Sandra Millen (University of British Columbia), Dr Juan Lucas Cervera (Universidad de Cádiz) and Dr James Davis Reimer (University of the Ryukyus) for invaluable comments. This study was partly supported by the International Graduate Program for the Asia-Pacific Region (University of the Ryukyus).

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