Symbiosis DOI 10.1007/s13199-014-0289-8 Protection of host anemones by snapping shrimps: a case for symbiotic mutualism? AmberM.McCammon& W. Randy Brooks Received: 4 June 2014 /Accepted: 29 July 2014 # Springer Science+Business Media Dordrecht 2014 Abstract The sea anemone Bartholomea annulata is an eco- especially common in marine environments (Roughgarden logically important member of Caribbean coral reefs which host 1975; Poulin and Grutter 1996;Côté2000). Mutualism; a a variety of symbiotic crustacean associates. Crustacean type of symbiotic relationship in which both partners derive exosymbionts typically gain protection from predation by dwell- some benefit from the association, are also widespread across ing with anemones. Concurrently, some symbionts may provide taxa (Boucher et al. 1982). The benefit(s) of symbiont- protection to their host by defending against anemone predators mediated protection of host species from microbial disease, such as the predatory fireworm, Hermodice carunculata,which parasites, and predators is increasingly evident (Haine 2008). can severely damage or completely devour prey anemones. Protection mechanisms are diverse and include various sym- Herein we show through both field and laboratory studies that biont derived chemical defenses (Haine 2008) as well as anemones hosting the symbiotic alpheid shrimp Alpheus armatus maintenance behaviors (Heil and McKey 2003; Stier et al. are significantly less likely to sustain damage by H. carunculata 2012) and defensive social interactions (Glynn 1980; Brooks than anemones without this shrimp. Our results suggest that the and Gwaltney 1993; Heil and McKey 2003;McKeonetal. association between A. armatus and B. annulata, although com- 2012). Previous studies have demonstrated that some crusta- plex because of the numerous symbionts involved, may be closer ceans will actively defend host cnidarians in their natural to mutualism on the symbiotic continuum. marine (Smith 1977; Glynn 1980) and laboratory settings (Brooks and Gwaltney 1993;McKeonetal.2012). Some Caribbean cnidarians are well studied due to their Keywords Alpheus . Anemone . Bartholomea . Fireworm . importance as focal locale for marine cleaning symbiosis, Hermodice . Shrimp symbionts though concentration has been on the interactions between visiting client fish that has ectoparasites removed by an unre- lated cleaner organism which generally associates with a 1 Introduction cnidarian host (Losey 1972; Van Tassell et al. 1994;Côté 2000; Floeter et al. 2007). Some anemone-dwelling shrimps Symbiotic interactions have been reported from a wide range have been reported to engage in marine cleaning symbiosis, of taxa (Dickman 1992;PoulinandVickery1995) and are eating parasites from fish in captivity (Bunkley-Williams and Williams 1998; Becker and Grutter 2004; Östlund-Nilsson Electronic supplementary material The online version of this article et al. 2005;McCammonetal.2010) and appear to remove (doi:10.1007/s13199-014-0289-8) contains supplementary material, which is available to authorized users. ectoparasites from free-living reef fishes (Côté 2000;Sikkel et al. 2004; Huebner and Chadwick 2012a). There is evidence A. M. McCammon that client fish and cleaner organisms benefit from the University of the Virgin Islands, John Brewers Bay, St Thomas, VI 00802, USA cleaning station association, however, whether the anemone e-mail: [email protected] host benefits from the anemone-crustacean symbioses is un- clear. Despite the potential importance of anemones as con- : * A. M. McCammon W. R. Brooks ( ) spicuous base stations for fish cleaning activity on coral reefs Florida Atlantic University, 777 Glades Road, Boca Raton, FL 33431, USA (Côté 2000; Humann and Deloach 2003; Huebner and e-mail: [email protected] Chadwick 2012b) few quantitative research studies exist on A.M. McCammon, W.R. Brooks patterns of abundance, symbiont diversity, or importance of Although defense by shrimp and crab associates of cnidar- crustacean macrosymbionts for the host sea anemone. ians has been demonstrated (Glynn 1980;Brooksand One of the largest and most common sea anemones on Gwaltney 1993), only one study has reported that a crustacean Caribbean coral reefs is the corkscrew anemone Bartholomea associated with B. annulata will display defensive behavior in annulata (LeSueur, 1817), which hosts a variety of crustacean the presence of an anemone predator (Smith 1977). The exosymbionts (Criales 1984) the majority of which are from amphinomid polychaete, bearded fireworm, Hermodice multiple families within Order Decapoda, that can inhabit a carunculata (Pallas, 1766), is a known cnidarian predator host anemone as solitary or mated pairs and as aggregations of (e.g., Witman 1988; Vreeland and Lasker 1989 ; Souza et al. individuals of mixed species (Calado et al. 2007). Derived 2007) that has been documented to eat solitary anemones host-symbiont recognition and acclimation mechanisms seem (Lizama and Blanquet 1975) including B. annulata (Smith to be species specific (Crawford 1992) and are currently 1977). H. carunculata hasbeenreportedtoforagediurnally unknown for many B. annulata associates. Decapod symbi- (Witman 1988) and nocturnally (Fine et al. 2002; Genovese onts such as the purple Pederson shrimp, Ancylomenes and Witman 2004)feedingonB. annulata by everting its pedersoni (Chace, 1958) (formerly within genus buccal mass over the anemone tentacles partially or complete- Periclimenes (Okuno and Bruce 2010)), the spotted cleaner ly eating the anemone down to the pedal disk (Pers. Obs.). shrimp, Periclimenes yucatanicus (Ives, 1891), and the red Damaged anemones exude defensive white threadlike acontia snapping shrimp, Alpheus armatus (Rathbun, 1901), are obli- with cnidae (Smith 1977, Pers. Obs.). gate associates that remain with the same host anemone for Most of B. annulata’s crustacean associates are relatively life and preferentially choose their natural host over other small and cryptic making it difficult to investigate interactions anemone species (Knowlton and Keller 1985, 1986; between these benthic invertebrates in the field without po- Gwaltney and Brooks 1994; Silbiger and Childress 2008). tentially influencing behaviors. Setting up assemblages simi- A. pedersoni is generally a non-aggressive, anemone-shrimp lar to those documented in the natural community facilitated that is an effective cleaner organism for reef fishes (Bunkley- observation and documentation of interspecific interactions. Williams and Williams 1998;McCammonetal.2010). In situ and laboratory microcosm experiments were conducted P. yucatanicus may be a cleaner mimic (McCammon et al. to test predictions of the hypothesis that anemone associates 2010) with similar morphological and behavioral characteris- play a deterrent or predator protection role for their host tics as A. pedersoni. A. armatus is an anemone-shrimp known anemone. for its aggressive territoriality, especially with non-mated con- specifics (Knowlton and Keller 1982;Hughes1996). Other crustaceans symbionts of B. annulata are facultative associ- 2Materialsandmethods ates which do not rely on a single anemone host throughout their life (Guo et al. 1996). The arrow crab, Stenorhynchus 2.1 Study localities seticornis (Herbst, 1788), is common on Caribbean reefs (Humann and Deloach 2002)andhasbeenreportedtoasso- Field experiments were carried out between July, 2008 and ciate with anemones (Herrnkind et al. 1976; Wirtz et al. 2009). March, 2010 in three shallow water (1–5 m) coral reef field S. seticornis may be a facultative symbiont of B. annulata localities in two south shore bays of the U.S. Virgin Islands; (Chadwick pers. Comm.) and is known anecdotally in the Donkey Bite Reef (DB) in Great Lameshur Bay on St. John aquarium trade to eat polychaetes, such as fireworms. (18°18′51″N, 64°43′16″W), Black Point Reef (BP), (18°20′ The anemone-crustacean association imparts some bene- 37″N, 64°58′54″W), and Ratchford Reef (RR), (18°20′24″N, fit(s) to both the host and its symbionts. Crustaceans that dwell 64°58′44″W), in Brewers Bay on St. Thomas. Multiple study with anemones can provide their host with nitrogenous waste localities were used for field experiments to investigate broad that fertilize endosymbiotic zooxanthellae, increasing the patterns across multiple bays. Donkey Bite and Black Point number of zooxanthellae cells (Spotte 1996) and potentially Reef are predominately Orbicella annularis complex coral increasing algal photosynthesis derived food supply for the beds and Ratchford Reef is a small patch reef. Laboratory anemone (Spotte 1996;PoratandChadwick-Furman2005). experiments were conducted within 25×30×33 cm, aquaria Shrimp may gain a food source while maintaining the host set in an outdoor wet table with open seawater flow at The anemone by removing excess mucus, necrotic tissue, and University of the Virgin Islands, McLean Marine Science inorganic debris (Herrnkind et al. 1976; Nizinski 1989; Center, on St. Thomas. Crawford 1992). Due in part to its large polyp size, fleshy tentacles and relatively toxic nematocysts, B. annulata may 2.2 Organism collection serve as protective host for facultative and obligate crustacean symbionts (Mihalik and Brooks 1995). Is the role of protector Species identification for all organisms was made using refer- reciprocal? ence materials (Fauchald 1973; Knowlton and Keller 1985; Protection of host anemones by snapping shrimps Spotte 1997;Campetal.1998; Humann and Deloach 2002; Microscopic examination of the stomach contents