Introduction

Several organisms are known to prey on sea slugs (Gastropoda: Opisthobranchia), including fish, crabs, worms and sea spiders (e.g. Trowbridge 1994; Rogers et al. 2000; Arango and Brodie 2003). The available information on sea slug predators nevertheless remains scarce (Rudman 2000).

Herein we report the first in situ observations of reef-dwelling sea anemones (Anthozoa: Actiniaria) attempting to feed on nudibranchs. There are no previous field observations of nudibranch predation by sea anemones, except for two records obtained through aquarium experiments (Thompson 1960; Bryan et al. 1998).

Material and methods

The observations were made during fieldwork on coral reefs in the Semporna district (eastern Sabah, Malaysia), as part of the Semporna Marine Ecological Expedition in December 2010 (SMEE2010). The reported observations were made on Creach Reef (04°18′58.8″N, 118°36′17.3″E) and Pasalat Reef (04°30′47.8″N, 118°44′07.8″E), at approximately 10 m depth for both observations. The nudibranch identifications were checked against Gosliner et al. (2008), whereas the identification of the sea anemone was done by A. Crowther. No material was collected. Photos were taken with a Canon 400D with a Sigma 50-mm macro lens.

Results

A reef-dwelling anemone, belonging to a species of the family Edwardsiidae, was observed on Creach Reef while attempting to feed on a nudibranch of the species Nembrotha lineolata Bergh, 1905 (family Polyceridae). On discovery, the nudibranch was ingested from its tail to gills (Fig. 1a) with the sea anemone’s mouth protruding around the nudibranch. The nembrothid was stretching its body and reaching in the direction of the sandy substrate (Fig. 1b–c). Meanwhile, the actininarian’s tentacles touched the nudibranch, making it flinch upon contact before continuing to stretch. Eventually, the nembrothid managed to pull itself free, leaving behind a thick mucus trail (Fig. 1d), while visually appearing unharmed (Fig. 1e). Subsequently, the anemone’s oral disc slowly retracted. The total observation time was about 7 min (Fig. 1a–e).

Fig. 1
figure 1

a–e The unsuccessful attempt of an edwardsiid sea anemone to feed on a Nembrotha lineolata. f A non-responsive Phyllidia ocellata caught by the tentacles of an edwardsiid sea anemone

Full size image

On a separate occasion, on Pasalat Reef, a different specimen of presumably the same edwardsiid species was observed holding a Phyllidia ocellata (Cuvier, 1804) (family Phylidiidae) upside down (Fig. 1f). The nudibranch was not responding to the sea anemone’s tentacles and appeared paralyzed or dead. The sea anemone was actively moving its tentacles, suggesting movement of its prey into the gastrovascular cavity. It is unknown if the ingestion was concluded successfully. The observation time was about 1 min.

Discussion

Sea slugs, informally grouped as the Opisthobranchia, are subdivided into numerous (sub-)clades, including the Aplysiomorpha (sea hares), Sacoglossa (sap-sucking slugs), and the large subclade of the Nudibranchia (true nudibranchs) (Bouchet and Rocroi 2005). Predation by sea anemones has only been reported for the Aplysiomorpha (e.g. Winkler and Tilton 1962; Johnson and Willows 1999). For the Sacoglossa there are records of predatory attacks by other sea slugs, as well as feeding experiments with fish and crabs (Trowbridge 1994). The majority of the predation records for the subclade Nudibranchia consist of attacks by other sea slugs (Rudman 2000).

Sea anemones are sedentary organisms, and are considered opportunistic feeders; their diet includes crabs, fish, sea urchins and zooplankton (Ruppert et al. 2004). The sea anemone in Fig. 1 is identified as belonging to the family Edwardsiidae, although it has been erroneously referred to as Condylactis sp. (e.g. Colin and Arneson 1995: fig. 565; Fosså and Nilsen 1998: p. 240). Edwardsiid sea anemones are common elements of the benthic marine infauna, but the Pacific actiniarian fauna is poorly known (Daly and Ljubenkov 2008). It is unclear whether nudibranchs form a major part of their diet. Dozens of other edwardsiid anemones were observed over the course of the 3-week fieldwork period, not increasing the number of predation records. The attempted predation of a phyllidid nudibranch is surprising because sea slugs of the Phyllidiidae are known to be toxic (Fusetani et al. 1992).