Host Selection by the Cleaner Shrimp Ancylomenes Pedersoni: Do Anemone Host Species, Prior Experience Or the Presence of Conspecific Shrimp Matter?
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Journal of Experimental Marine Biology and Ecology 413 (2012) 87–93 Contents lists available at SciVerse ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Host selection by the cleaner shrimp Ancylomenes pedersoni: Do anemone host species, prior experience or the presence of conspecific shrimp matter? Maite Mascaró a,⁎, Lizbeth Rodríguez-Pestaña b, Xavier Chiappa-Carrara a, Nuno Simões a a Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, Universidad Nacional Autónoma de México, Sisal, Yucatán, México b Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, México D.F. México article info abstract Article history: In the symbiotic association that exists between cleaner shrimp Ancylomenes pedersoni (=Periclimenes peder- Received 13 February 2011 soni) and host sea anemones, specificity varies among populations, and shrimp are believed to search among Received in revised form 23 November 2011 different individual hosts for favourable positions from which to attract client fish. Four laboratory-based exper- Accepted 25 November 2011 iments were conducted to test host selection of A. pedersoni between the following: i) Bartholomea annulata Available online xxxx (corkscrew anemone) and Condylactis gigantea (condy anemone), ii) B. annulata, with or without a conspecific resident, iii) a previously known or unknown B. annulata, and iv) a previously known or unknown C. gigantea. Keywords: Ancylomenes (=Periclimenes) pedersoni Preference (active selection) was distinguished from mere passive association by comparing shrimp acclimation Bartholomea annulata to anemones offered in choice and no-choice (control) situations. The results were analysed using asymmetrical Cleaner shrimp χ2 contingency tables (in each experiment, n=60) where expected frequencies were obtained with maximum Condylactis gigantea likelihood estimators. Shrimp acclimated more frequently to B. annulata than to C. gigantea, but they acclimated Preference similarly to anemones with or without another resident and to those B. annulata and C. gigantea anemones that Sea anemones were familiar rather than unfamiliar. However, none of the χ2 values were statistically significant 2 (χ df = 1 =0.48, 0.19, 0.42, 0.42; overall p>0.45), suggesting that preference may not be responsible for the as- sociation between adult A. pedersoni and its host anemones observed in the field. Differences in the frequency of association may be due to factors other than the active decisions made by shrimp when presented with more than one alternative host. © 2011 Elsevier B.V. All rights reserved. 1. Introduction the degree to which resident shrimp are host-specific varies with both the shrimp and host species and can differ from one population to an- Several species of the shrimp genus Periclimenes establish symbiotic other within the distribution range (Silbiger and Childress, 2008 and relationships with sea anemones, but the costs and benefits of such examples therein). associations are still uncertain (Bauer, 2004; Fautin et al., 1995). Ancylomenes pedersoni (Chace, 1958) (reported as Periclimenes ped- While some studies suggest commensalism where only shrimp obtain ersoni until recently; Okuno and Bruce, 2010) is distributed from Cape protection from predators (Bruce, 1976), other studies consider mutu- Lookout, North Carolina, down the east coast of the United States and alism as the basis for the interaction in which anemones obtain either around the west coast of Florida, to the Bahamas, West Indies, Bonaire, protection from shrimp (McCammon, 2010) or an additional source of Netherland Antilles and Belize (Chace, 1958, 1972; Williams, 1984). nitrogen from shrimp faeces (Spotte, 1996). Field studies report A. pedersoni to be a symbiotic cleaner shrimp Differences in the degree of host specialisation can be mediated by frequently associated with Bartholomea annulata, to a lesser extent habitat use because some of these species are considered to be cleaner with Condylactis gigantea, and occasionally with other anemones shrimp that remove parasites and decayed tissue off of client fish (Chace, 1972; Mahnken, 1972; Silbiger and Childress, 2008; Williams (Kotter, 1997; Limbaugh et al., 1961; Mahnken, 1972; Zhang et al., and Bunkley-Williams, 2000). However, in Quintana Roo, Mexico, 1998). In general, Periclimenes (sensu lato) that do not clean fish are A. pedersoni has never been observed to be associated with C. gigantea considered to be host-specific, whereas cleaner shrimp search among (Campos-Salgado, 2009), although several authors have reported this different anemone species for favourable positions from which to specific association at other locations in the Great Caribbean (Criales attract fish (e.g., Feder, 1966; Guo et al., 1996; Limbaugh et al., 1961; and Corredor, 1977; Mihalik, 1989; Spotte et al., 1991; Wicksten, Nizinski, 1989; Williams, 1984). Moreover, as in other associations, 1995) and the Gulf of México (Sisal Banks and Alacranes Reef; Simoes, N., pers. obs.). There is also considerable variation in the grouping pattern exhib- ⁎ Corresponding author. Tel./fax: +52 988 9120147. ited by cleaner shrimp of the genus Periclimenes. Several authors E-mail address: [email protected] (M. Mascaró). mention that A. pedersoni are often found alone, in pairs, or in groups 0022-0981/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2011.11.026 88 M. Mascaró et al. / Journal of Experimental Marine Biology and Ecology 413 (2012) 87–93 of 5–6 individuals (Mahnken, 1972; Stanton, 1977). In the Mexican of different sizes and reproductive conditions described for the Mexican Caribbean (Campos-Salgado, 2009; unpublished data), 63% of the Caribbean (Campos-Salgado, 2009), only A. pedersoni (1.5-2.5 cm B. annulata recorded had no A. pedersoni, 21% had 1 individual, 9% had length), B. annulata and C. gigantea (5–10 cm diameter of the oral disc 2 individuals, and 7% had groups of 3–5 shrimp. Groups of more than of completely distended anemones) were used in the experiments. 10 shrimp of different sizes that are associated with only one host The sex of captured shrimp was not recorded, but all individuals were have occasionally been observed (Campos-Salgado, 2009; Wicksten, non-ovigerous. Shrimp were captured using fine nets, and anemones 1995). There have been reports of considerable aggression between were carefully removed from the substratum to minimize damage to individuals competing for favourable positions within a host to obtain animals and reefs. Taxonomic descriptions by Chace (1972) and food, both under laboratory conditions and in the wild (Mahnken, Gonzalez-Muñoz (2008) were used to correctly identify shrimp and 1972). While these observations suggest that shrimp that are already anemone species, respectively. Captured organisms were individually present in an anemone may constitute an adverse stimulus for other placed in small plastic containers, previously perforated to allow A. pedersoni to acclimate to that particular host, previous residents water exchange. The containers were kept in a large plastic holder could act as positive stimuli and attract more individuals. Huebner with abundant seawater and constant aeration to ensure survival dur- (2010) reported that the number of fish being cleaned at any particular ing transportation to the Unidad Multidisciplinaria de Docencia e Inves- station increased significantly with the number of A. pedersoni associat- tigación, Facultad de Ciencias, Universidad Nacional Autónoma de ed to the host. This suggests an advantage for client fish to stop at anem- México, at Sisal, Yucatán, México where experiments were conducted ones that host several shrimp. However, for such gregarious behaviour from September 2007 to March 2008. An identification code was to constitute an advantage for A. pedersoni,individualshrimpwould assigned to each individual to make it possible to retrieve detailed infor- need to benefit from the aggregation (e.g., if the mean rate of food intake mation about its capture. Hosts and anemones captured at the same per individual shrimp increased in stations with several A. pedersoni location were never used in the same trial to prevent previous contact compared with those with only one or two shrimp). between the host and the shrimp from potentially affecting selective Symbiotic decapods associated with sessile marine macroinverte- behaviour. To comply with statistical independence, individual shrimp brates live in well-established microhabitats (i.e., sessile hosts; Baeza were used only once in the same experiment. Anemones were used and Stotz, 2003), and the shrimp-anemone relationship constitutes an several times in the same experiment, but were isolated for 15 days be- ideal model to study host preference. However, the associations that tween subsequent trials. A. pedersoni that were separated from both are often observed in natural conditions do not necessarily reflect B. annulata and C. gigantea for 15 days have been shown to lose protec- preference for a particular host species or individual because their dis- tion from the nematocysts of these anemones, but re-acclimate if tribution may be the result of ecological factors, such as host abundance, allowed contact with hosts (Rodriguez-Pestaña, 2007). or inter- and intra-specific competition and predation (Gwaltney and Shrimp and anemones were isolated and maintained in fibre-glass Brooks, 1994; Khan et al., 2003; Silbiger and Childress,