BULLETIN OF MARINE SCIENCE, 78(2): 281–286, 2006 ADELOMELON BRasILIANA anD ANTHOLOba ACHATES: A PHoretic association betWeen A VolutiD GastroPOD anD A sea anemone in ARGentine Waters Diego Luzzatto and Guido Pastorino Abstract We describe a phoretic relationship between Adelomelon brasiliana (Lamarck), a common gastropod (Volutidae) along the coast of the province of Buenos Aires, and the sea anemone Antholoba achates (Drayton). Ninety-five percent of the sampled gastropods participate in this association, with the remaining 5% juvenile speci- mens. In order to discover a preferential position of anemone attachment and to assess the frequency of this association, the gastropod shell was divided into three approximately equal sectors and the anemones in each sector counted. The maxi- mum number of anemones attached on the dorso-abaxial side near the aperture. Despite the high frequency of anemones on the shell of A. brasiliana, results suggest that only the anemone benefits from this association. There is extensive literature on the association between sea anemones and her- mit crab shells (e.g., Ross, 1960; Ross and Sutton, 1961a,b; Ross and Zamponi, 1983; Brooks and Mariscal, 1986), while studies of the symbioses between anemones and gastropods are scant (reviewed by Ates, 1995, 1998). Few authors mention the rela- tionship between living gastropods and sea anemones in the southern Atlantic and Pacific oceans. Riemann-Zürneck (1980) studied the apparently obligate bond of Isosicyonis alba (Studer, 1878) to several species of gastropods. Bellisio et al. (1972) and Arnaud (1978) reported a symbiosis between the volutid Harpovoluta charcoti (Lamy, 1910) and I. alba from Antarctic waters. As far as we know, the volutes Provo- cator corderoi (Carcelles, 1947) and H. charcoti are the only reported gastropods that participate as substrate in this anemone-gastropod association. In Japan, Ross and Kikuchi (1976) described the link between two anemones with the gastropods Sipho- nalia filosa (Adams, 1863) (Buccinidae), Hinia festiva (Powys, 1835), and Niotha livi- scens (Philippi, 1849), (Nassariidae). In Argentine waters, Pastorino (1993) described the phoretic association between the gastropod Buccinanops cochlidium (Dillwyn, 1817) and the sea anemone referred to as Phlyctenanthus australis Carlgren, 1949 from Puerto Pirámides, Chubut Province, and now thought to be Antholoba achates (Drayton in Dana, 1846). Acuña et al. (2003) described the same anemone living in a mutual relationship with the spider crab Libinia spinosa Milne Edwards, 1934. Carter (1965), in a catalogue of the anemones of central Chile, described the actinian A. achates as living on hard substrates and associated with gastropods of the genera Argobuccinum (Ranellidae) and Chorus (Muricidae). Despite the fact that the gastropod Adelomelon brasiliana (Lamarck, 1811) has been the target of a commercial fishery in Uruguay and Argentina for many years, there is no mention in the scientific literature of this gastropod-anemone associa- tion. Here we describe the symbiotic relationship of this common volutid and the sea anemone A. achates. Bulletin of Marine Science 281 © 2006 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 282 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 2, 2006 Materials and Methods Adelomelon brasiliana ranges from Rio de Janeiro, Brazil to the northern area of Golfo San Matías, Argentina (~41°S) and inhabits the coastal fringe between 10 and 70 m depth, always on sandy bottoms (Rios, 1994). However, along the coast of the province of Buenos Aires, it is found in 8–20 m depth. The sea anemone A. achates ranges from southern Brazil in the north to the Magellanic area in the Atlantic, and Chile in the Pacific (Carter, 1965; Riemann-Zürneck, 1986), where it is usually found living in the sublittoral zone. A sample of 55 A. brasiliana individuals was collected with a trawl net by fishermen off the coast of Mar del Plata (~38°S). Gastropods and their attached anemone(s) were counted and measured with a caliper. The measurements taken on the gastropods were maximum height and apertural length. For anemones, the maximum and minimum diameter of the pedal disk and column were measured. In addition, the position and number of anemones were mapped on the shell that was divided into three sectors (Fig. 1C). Each sector corresponded to an equivalent topographic area of the shell. A logistic regression analysis was performed in order to establish preference distribution patterns of the anemone on the shell. The zones where the anemones were attached were considered as the independent variable, and the presence and absence of the anemone as the dependent variable. We also calculated a linear correlation between the sizes of the shell vs the number of anemones. Specimens housed at the Museo Argentino de Ciencias Naturales (MACN-20524), contain- ing several individuals of A. brasiliana with attached A. achates, were measured and photo- graphed (Fig. 1); these were outside of the sampled population and not used in the statistical analysis. Results Adelomelon brasiliana is a large gastropod of about 20 cm of shell maximum height and 11 cm width, with a quadrangular profile. The shell is about 2–3 mm thick at the edge of the aperture. The spire is usually very low and nodulose, and the last whorl is the largest. As in most volutids, there is no operculum; the aperture is closed by a thick foot. A long siphon (Fig. 1E) allows the gastropod to remain buried under the sand for a somewhat extended period. At the same time the associated anemone subsists attached to the gastropod, but above the sand-water interface (Fig. 1D). The largest recorded specimen of A. achates attached to A. brasiliana had an oral disc diameter > 12 cm and a column height of about 5 cm. The anemone usually cov- ered the whole shell including the last whorl and spire. Ninety-five percent of the 55 gastropod specimens sampled participated in this association. The snails sampled ranged from 2 to 18 cm maximum height. All snails without anemones were < 3 cm maximum height. The maximum number of anemo- nes recorded per shell was seven (Fig. 1A,B), but 60% of the gastropods had only one anemone attached (Fig. 2). The number of anemones per shell was significantly related to the gastropod size (R2 = 0.25, P = 0.003; Fig. 3). Among the museum speci- mens, we recorded an extraordinary case of 12 anemones living on one large shell of the gastropod (MACN 20524). Sector 1 of the gastropod had the maximum number of anemones attached. (Lo- gistic regression: Nagelkerke R2 = 0.44, P < 0.001). Eighty-six percent of the snails sampled had at least one anemone in sector 1, while the 27% and 17% had anemone(s) in sectors 2 and 3, respectively. In 95% of the snails, sector 1 had no epibiont other than the anemone, while in 80% of snails sectors 2 and 3 had other kinds of epibionts LUZZATTO AND PASTORINO: ASSOCIATION BETWEEN A GASTROPOD AND A SEA ANEMONE 283 Figure 1. A) Apertural and B) dorsal view of a preserved specimen of Adelomelon brasiliana with seven attached specimens of Antholoba achates (MACN 20524) from the mouth of Rio Negro (~40°S). C) Dorsal view of another specimen (MACN 20524) with six attached specimens of A. achates; three sectors of the shell surface are shown. D) The disk of a living A. achates speci- men when the gastropod is buried in the sand. Arrowhead indicates the sand around the anemone column. E) Lateral view of a living A. brasiliana with a large sea anemone attached; arrowhead points to the tip of the extended siphon. 284 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 2, 2006 Figure 2. Frequency of attached anemones (Antholoba achates) per gastropod (Adelomelon brasiliana) shell. whether or not they had anemones. In several cases, we found barnacles, bryozoans, and/or polichaetes under the attached anemone, although most of them were prob- ably dead. This suggests that the anemone is capable of moving over the entire shell surface despite the presence of epibionts. Discussion Our results, together with those of Carter (1965), suggest that A. achates has no specific preference for gastropod species. Carter (1965) found 80% of livingArgobuc - cinum sp. (Ranellidae) specimens to be associated with anemones at 13 m depth off central Chile. We found ~95% of A. brasiliana associated with the same anemone off Argentina. The likely benefits to the actinian are the attachment substrate and phoresy provid- ed by the gastropod with the consequent ability to live and move on soft substrates. In contrast, the benefits derived from this association for the gastropod are less clear. The usual explanation is protection from predators. Arnaud (1978) suggested thatH . charcoti benefits from its association withI . alba in that the small shell of H. charcoti Figure 3. Number of attached anemones (Antholoba achates) as a function of maximum gastro- pod (Adelomelon brasiliana) shell height. LUZZATTO AND PASTORINO: ASSOCIATION BETWEEN A GASTROPOD AND A SEA ANEMONE 285 apparently does not fully cover the soft parts of the animal; therefore, the anemone may play an important role in protecting the gastropod. The shell of H. charcoti has a thickness of 1.1 mm, decidedly thinner than the shell of A. brasiliana of the same size (2.7 mm). Furthermore, the shell of A. brasiliana entirely covers the soft parts in retraction. Such a retraction pulls the foot in well beyond the aperture. Therefore, protection by the sea anemone is unlikely in this association. Immediately after the strong storms locally known as “Sudestada” (which include gale-force winds from the southeast and also increased swell), live A. brasiliana can be found on the beach with their sea anemones still attached. We suspect that the presence of the anemones on the shell may contribute to their dislodgement from the bottom onto the coast.