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Crustacean Biology Advance Access Published 6 November 2019 Journal of Crustacean Biology the Crustacean Society Journal of Crustacean Biology 40(1), 24–36, 2020

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Crustacean Biology Advance Access Published 6 November 2019 Journal of Crustacean Biology the Crustacean Society Journal of Crustacean Biology 40(1), 24–36, 2020 applyparastyle "fig//caption/p[1]" parastyle "FigCapt" applyparastyle "fig" parastyle "Figure" Journal of Crustacean Biology Advance Access published 6 November 2019 Journal of Crustacean Biology The Crustacean Society Journal of Crustacean Biology 40(1), 24–36, 2020. doi:10.1093/jcbiol/ruz081 Social behavior of the Pederson cleaner shrimp Downloaded from https://academic.oup.com/jcb/article-abstract/40/1/24/5613990 by Auburn University user on 13 January 2020 Ancylomenes pedersoni (Chace, 1958) (Decapoda: Caridea: Palemonidae) in the Caribbean Sea: size- and gender-based dominance hierarchy Jessica A. Gilpin and Nanette E. Chadwick Department of Biological Sciences, 101 Rouse Life Sciences Building, Auburn University, Auburn, AL 36849, USA Corresponding author: J.A. Gilpin; e-mail: [email protected] (Received 5 June 2019; accepted 10 October 2019) ABSTRACT Social interactions among Pederson cleaner shrimp Ancylomenes pedersoni (Chace, 1958), an as- sociate of sea anemones, likely affect cleaning services to reef fishes, but major aspects of their social group structure and behavior remain unknown. We hypothesized that Pederson shrimp form dominance hierarchies expressed through size- and gender-based behavioral inter- actions. Observation of 116 shrimp on coral reefs at St. Thomas, US Virgin Islands, revealed that they formed social groups of ~3 or 4 individuals (range 1–9) per host sea anemone, as a mix of large females, medium-size males, and/or small juveniles. Social groups were not rigidly size-structured, in that body size ratio between adjacent individuals did not differ sig- nificantly from random. Individuals, however, were spatially structured such that distance be- tween shrimp and the tentacles of the host anemone decreased significantly with shrimp body size; large individuals occupied the anemone tentacle crown, whereas smaller shrimp perched on reef or sand substrates adjacent to the anemone. During laboratory experiments, shrimp exhibited five types of exploitation competition behaviors toward client fish models (signal, approach, clean, no response, retreat), and four types of interference competition behaviors toward conspecific shrimp (approach, attack, no response, retreat). Large females more fre- quently signaled toward, approached, and cleaned fish models than did males and juveniles, which did not respond or retreated. Females also approached and attacked conspecifics more than did males and juveniles, which retreated at frequencies that increased with decreasing body size. We conclude that Pederson shrimp form gender and size-based hierarchies in which large females monopolize food resources (ectoparasites on client fishes), and interfere with re- source access by smaller males and juveniles. These behaviors cause them to spatially partition microhabitats on anemones, and hypothetically could lead to males and juveniles dispersing among anemones more frequently than females. These shrimp social interactions may thus enhance spatial and temporal variation among cleaning stations, with consequences for the health and mobility of reef fishes. Key words: anemone shrimps, aggression, behavior, cleaning symbiosis, coral reefs, coral reef fishes, habitat segregation, sea anemones INTRODUCTION associates of corkscrew anemones. The shrimp also associates with other Caribbean sea anemones, including rosetip anemones Corkscrew sea anemones Bartholomea annulata (Le Sueur, 1817) are Condylactis gigantea Weinland, 1860, branching anemones Lebrunia common, large-bodied Caribbean cnidarians that host a variety danae (Duchassaing & Michelotti, 1861), and sun anemones of associated organisms on, among, and beneath their tentacles Stichodactyla helianthus (Ellis, 1768). The Pederson shrimp perch on (Mahnken, 1972; Brooker et al., 2019). The Pederson cleaner the oral discs and tentacles of corkscrew anemones (Mahnken, shrimp Ancylomenes (Periclimenes) pedersoni (Chace, 1958) are obligate 1972) and occupy reef crevices where these anemones attach © The Author(s) 2019. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: [email protected] SOCIAL BEHAVIOR OF CLEANER SHRIMP their pedal disks (Limbaugh et al., 1961). These large anemones the “aggressive state” of other group members may be a stronger serve as visual cues that attract reef fishes, which then engage determinant of social status than individual recognition (Winston in cleaning interactions with the shrimp (Huebner & Chadwick, & Jacobson, 1978). Aggressive interactions are known to struc- 2012a). Client fishes may in turn provide excreted nutrients that ture arthropod social hierarchies, including crickets (Alexander, benefit the anemone and its endosymbiotic microalgae (Cantrell 1961), hermit crabs (Courchesne & Barlow, 1971), and crayfishes et al., 2015). On branching anemones L. danae, the shrimp typ- (Bovbjerg, 1953; Rubenstein & Hazlett, 1974; Copp, 1986; Issa ically perch on reef substrate within a few centimeters of the et al., 1999). diurnally-expanded fronds of host anemones, or rest atop the In addition to aggressive state, relative body size also contrib- fronds (Herrnkind et al., 1976). The shrimp-anemone complex utes to determination of the outcome of conflicts among conspe- forms a cleaning station, where shrimp consume parasites and cifics (Bovbjerg, 1953; Ranta & Lindström, 1992; Pavey & Fielder, decayed tissue from the body surfaces of fishes that visit the 1996). Large Pederson shrimp may occupy more central positions anemone (Bunkley-Williams & Williams, 1998; Côté, 2000). on anemones than do small shrimp (JG, personal observation), Downloaded from https://academic.oup.com/jcb/article-abstract/40/1/24/5613990 by Auburn University user on 13 January 2020 Pederson shrimp aggregate in social groups (as defined by Costa potentially indicating a spatially structured social hierarchy based & Fitzgerald, 2005) ranging from 1–12 shrimp per host anemone in part on relative body size, similar to the pattern observed for (Mahnken, 1972, Titus et al., 2015), with individuals in each so- other anemone shrimps (Colombara et al., 2017). The prominent cial group varying in body size (Mahnken, 1972; Mascaró et al., habitats occupied by large individuals could be due not only to 2012). Researchers have speculated that the number of Pederson interference with smaller shrimp, but also to exploitation competi- shrimp in each social group depends on habitat space availability tion for access to client fishes and thus food resources in the form on the anemone host, as well as on the abundance of the local of parasites and decayed fish tissue (Mascaró et al., 2012). The shrimp population; space limitation (host anemone abundance mechanism of exploitation competition utilized by large shrimp is and body size) is thus thought to be more important in con- potentially via signaling to and approaching fish clients more fre- straining the abundance of this species than in other non-group- quently than do small shrimp, which would allow them to monop- forming shrimps associated with Caribbean anemones (Mahnken, olize food resources in the form of fish ectoparasites before small 1972; Nizinski, 1989). Recent analyses have confirmed that larger individuals can access them. corkscrew anemones, which provide more habitat space, host sig- We hypothesized that Pederson shrimp form social dominance nificantly more Pederson shrimp than do smaller anemones (Titus hierarchies based on the outcomes of size- and gender-based be- et al., 2017; Huebner et al., in press). In contrast, the number of havioral interactions. Our objectives were to test this hypothesis by shrimp per anemone does not appear to vary with their frequency quantifying 1) the structure of social groups observed under field of cleaning or cheating behaviors toward fish clients (Titus et al., conditions, and 2) the behaviors of shrimp in experimental social 2015, 2019). A size-dependent dominance hierarchy has been pro- groups under laboratory conditions. posed to structure social groups of Pederson shrimp (Mahnken, 1972), but no quantitative data support this idea. Many studies have described the important functional role of MATERIALS AND METHODS cleaning stations in coral reef ecosystems, including how cleaner Field observations organisms enhance health and abundance of reef fishes (Bunkley- Williams & Williams, 1998; Bshary, 2003; Becker & Grutter, 2004, Field observations were conducted during July 2015 and August 2005; Bshary et al., 2007), and how fishes use cleaning stations 2016 on patch reefs in Brewers Bay, St. Thomas, U.S. Virgin (Chapuis & Bshary, 2009; Huebner & Chadwick, 2012b; Titus Islands, at ~6 m depth (18°19′N, 64°59′W; detailed site descrip- et al., 2015, 2017, 2019; Caves et al., 2018). Analyses of behavioral tions in Gilpin & Chadwick, 2017; Huebner & Chadwick, 2012a, interactions between cleaner shrimps and their cnidarian hosts, b; O’Reilly et al., 2018; Huebner et al., in press). We conducted and of cleaner shrimp life histories, are nevertheless lacking outside preliminary observations to locate reef areas that were within or of host preference and acclimation studies (Levine & Blanchard, near those examined in the above studies, and which contained 1980; Guo et al., 1996; Silbiger & Childress, 2008; Mascaró et al., high abundances of corkscrew sea anemones and associated 2012) and one population study of non-cleaner shrimp Periclimenes Pederson shrimp. Other species of large coral reef sea anem- anthophilus
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