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Interspecific Variation in Anemone Shrimp Distribution and Host Selection in the Florida Keys (USA): Implications for Marine Conservation

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Interspecific Variation in Anemone Shrimp Distribution and Host Selection in the Florida Keys (USA): Implications for Marine Conservation BULLETIN OF MARINE SCIENCE, 83(2): 329–345, 2008 IntersPecific Variation in anemone SHrimP Distribution anD Host selection in THE FloriDA KEYS (USA): IMPlications FOR marine conserVation Nyssa J. Silbiger and Michael J. Childress Abstract Host and symbiont abundances often depend on the degree of host specificity and differences in costs and benefits of these associations. In this study, we investigated the distribution of anemone shrimps and their hosts along with the shrimps’ host selection behavior to evaluate the degree of host specificity in a nearshore benthic community undergoing rapid environmental change. We compared the distribution of two shrimp species, Periclimenes pedersoni Chace, 1958, and Periclimenes yu- catanicus (Ives, 1891), with their three anemone hosts, Condylactis gigantea (Wein- land, 1860), Stichodactyla helianthus (Ellis, 1767), and Bartholomea annulata (Le- sueur, 1817). The proportion of host anemones occupied by each shrimp species was significantly non-random considering abundance of each species per location and significantly different from a previous study conducted 18 yrs earlier. This was due to a decline in S. helianthus abundance. Periclimenes yucatanicus abundance was correlated with C. gigantea abundance, but P. pedersoni abundance was correlated with B. annulata abundance and all anemone species combined. A dichotomous choice test between C. gigantea and B. annulata revealed that P. yucatanicus select- ed C. gigantea regardless of its original host species. However, P. pedersoni selected its original host species. These results suggest that P. yucatanicus retains a strong host specificity for C. gigantea, whereas P. pedersoni appears to show no particular host specificity. Species with strong host specificity, such as P. yucatanicus, may be less likely to switch host species, and therefore, may be more susceptible to a decline in host abundance. Understanding the patterns and mechanisms of host specificity in symbiotic re- lationships is important to marine conservation. Symbionts may actually increase the health of corals and anemones by providing oxygen and nutrients (Spotte, 1996; Porat and Chadwick-Furman, 2004), protecting hosts from predators (Smith, 1977; Prachett et al., 2000; Prachett, 2001), and even cleaning tissues (Stewart et al., 2006). Understanding how these associations are formed and maintained especially during times of rapid environmental change is essential to our goal of maintaining healthy coral reef ecosystems. Symbiotic relationships, while prominent in marine ecosystems, present some unique challenges to marine conservation (Castro, 1988). What will happen to a symbiont if its host species declines or goes extinct? Does the degree of host speci- ficity indicate something about the probability of persistence when multiple host species are in decline? Does the mechanism of host selection determine which sym- bionts are most resistant to changes in host abundance? In this study, we explored the host specificity and host selection behavior of two species of anemone shrimps in the genus Periclimenes with three species of sea anemones in the shallow waters of Florida Bay within the Florida Keys National Marine Sanctuary (USA). Our goal was to understand how differences in host selection behavior, which we defined as an anemone shrimp preferentially choosing one anemone host species over another, Bulletin of Marine Science 329 © 2008 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 330 BULLETIN OF MARINE SCIENCE, VOL. 83, NO. 2, 2008 might influence the distribution of shrimps in the field and their resistance to chang- es in host abundance. A wide variety of decapod crustaceans, especially shrimps and crabs, are symbi- onts on mollusks, echinoderms, corals, and sea anemones (Wirtz, 1997; Baeza and Thiel, 2003; Bauer, 2004; Kahn et al., 2004). Coral and sea anemone hosts often ben- efit directly by protection against predators (Smith, 1977;P ratchett, 2001), decreased sedimentation (Stewart et al., 2006), or increased nitrogen from symbiont waste (Spotte, 1996). Shrimp and crab symbionts often benefit by protection from preda- tors (Vytopil and Willis, 2001) and feeding directly on the host tissue (Fautin et al., 1995). Some species occupy a wide range of different hosts Periclimenes( rathbunae Schmitt, 1924—Spotte et al., 1991; Allopetrolisthes spinifrons (H. Milne-Edwards, 1837)—Baeza and Stotz, 2001) while others tend to be found exclusively on a single host species (Periclimenes ornatus Bruce, 1969—Omori et al., 1994; Guo et al., 1996; Pinnotheres halingi Hamel, Ng and Mercier, 1999—Hamel et al., 1999). If the costs and benefits to host and symbiont vary by association, this would presumably influ- ence the degree of host specificity. Our study focuses on two anemone shrimp species, Periclimenes pedersoni and Periclimenes yucatanicus that are known to associate with multiple species of sea anemones, false corals, jellyfish, and clams (Table 1). Judging from the taxonomic diversity of their hosts, these species might be assumed to have relatively low host specificity, however, this varies geographically. For example, Nizinski (1989) re- ported that high host specificity occurs in Periclimenes anthophilus Holthius and Eibl-Eibesfeldt, 1964 [P. pedersoni; Wicksten (1995b) and Spotte (1999)] in Bermuda, because shrimps were only found in the giant anemone Condylactis gigantea even though other suitable anemones, such as Bartholomea annulata were available. Mahnken (1972) found nearly the opposite pattern of association in St. John, US Vir- gin Islands, with nearly all the P. pedersoni and a majority of P. yucatanicus found in association with B. annulata. Only a few studies have addressed the specific mechanisms of host selection and acclimation that might lead to host specificity (Table 2). Levine and Blanchard (1980) found that Periclimenes spp. obtain protection from their host anemones through a period of toxin acclimation where the shrimp picks up mucus from the anemone, thereby reducing its susceptibility to being stung by the host’s nematocysts. If a shrimp is separated from its host for > 3 d, it gradually loses this resistance (Crawford, 1992). Mihalik (1989) and Gwaltney and Brooks (1994) studied whether familiarity with a particular host species influenced host selection. They collected P. pedersoni and P. yucatanicus from three anemone hosts (B. annulata, C. gigantea, and Stichodactyla helianthus) at six locations in the Florida Keys and found that P. yucatanicus associ- ated mostly with S. helianthus and selected S. helianthus over either C. gigantea or B. annulata in dichotomous choice tests. In the past 18 yrs since the studies by Mihalik and Gwaltney and Brooks, the near- shore communities of Florida Bay have experienced a cascade of environmental per- turbations. Massive seagrass die-offs in the central portion of Florida Bay have led to increased nutrient levels and corresponding blooms of cyanobacteria (Roblee et al., 1991; Fourqurean et al., 1993). These dense algal blooms resulted in widespread de- cline of macroalgae, sponges, cnidarians, and juvenile lobsters (Chiappone and Sul- livan, 1994; Butler et al., 1995; Herrnkind et al., 1997). Table 1. Summary of known hosts of Caribbean anemone shrimps. Shrimp species Host species Location Citation silbiger 1Periclimenes anthophilus Actinia bermudensis McMurrich, 1889 Bermuda Holthuis and Eibl-Eibesfeldt, 1964; Holthuis and Eibl-Eibesfeldt, 1964 Chase, 1972 Condylactis gigantea (Weinland, 1860) Bermuda Holthuis and Eibl-Eibesfeldt, 1964; an Chase, 1972; Sargent and Wagen- D C bach, 1975; Nizinski, 1989 H il Periclimenes pedersoni Chace, 1958 Aiptasia pallida (Verrill, 1864) Santa Marta, Colombia Criales, 1984 D ress Antipathes pennacea Pallas, 1766 Bonaire, Netherlands Antilles Spotte, 1995 : Bartholomea annulata (Lesueur, 1817) Bahamas Limbaugh et al., 1961 anemone St. John, US Virgin Islands Mahnken, 1972 Antigua Chase, 1972 S St. Vincent Criales and Corredor, 1977 H rim Santa Marta, Colombia Criales, 1984 P D Pine Cay, Turks and Caicos Spotte et al., 1991 istribution St. Thomas, US Virgin Islands Spotte et al., 1991 Summerland Key, Florida Mihalik, 1989; Gwaltney and Brooks, 1994 Bonaire, Netherlands Antillies Wicksten, 1995a an Bunodosoma granulifer (Leseur, 1817) Santa Marta, Colombia Criales, 1984 D H Cassiopea xamachana Bigelow, 1892 Santa Marta, Colombia Criales, 1984 ost Cerianthus sp. Santa Marta, Colombia Criales, 1984 selection Condylactis gigantea (Weinland, 1860) St. Vincent Criales and Corredor, 1977 Pine Cay, Turks and Caicos Spotte et al., 1991 Long Key, Florida Mihalik, 1989; Gwaltney and in Brooks, 1994 flori Bonaire, Netherlands Antilles Wicksten, 1995a D Discosoma (Rhodactis) sanctithomae Lee Stocking Island, Bahamas Williams and Williams, 2000 A (Duchassiang and Michelotti, 1860) ba Y 331 332 Table 1. Continued. Shrimp species Host species Location Citation Heteractis lucida St. Vincent Criales and Corredor, 1977 Duchassaing and Michelotti, 1864 Lebrunia danae Grand Bahama, Bahamas Herrnkind et al., 1976 (Duchassaing and Michelotti, 1860) Santa Marta, Colombia Criales, 1984 Providenciales, Turks and Caicos Spotte et al., 1991 Lima scabra (Born, 1778) Exuma Cays, Bahamas Spotte, 1995 BULLETIN OF MARINE SCIENCE, Ricordea florida La Parguera, Puerto Rico Williams and Williams, 2000 (Duchassaing and Michelotti, 1860) Periclimenes rathbunae Schmitt, 1924 Bartholomea annulata (Lesueur, 1817) St. John, US Virgin Islands Mahnken, 1972 Bunodosoma granulifer
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