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To Sea Anemones BULLETIN OF MARINE SCIENCE. 30(2): 460-466. 1980 CORAL REEF PAPER ACCLIMATION OF TWO SHRIMPS OF THE GENUS PERICLIMENES TO SEA ANEMONES Daniel M. Levine and Orland J. Blanchard, Jr. ABSTRACT Through an acclimation behavior, Peric/imenes rathbunae Schmitt and Periclimenes an- thaphi/us Holthuis and Eibl-Eibesfeldt acquire protection from the tentacles of their respec- tive host sea anemones, Staichactis helianthus (Ellis) and Candy/actis gigantea (Weinland). Laboratory experiments have shown that after a period of isolation from the host these shrimps lose their protection from nematocysts. Unacclimated (=unprotected) shrimps were stung by anemones with and without shrimps living with them, while acclimated (=protected) shrimps were not stung by anemones, with or without shrimps. Many shrimp species belonging to the family Palaemonidae are found in sym- biotic association with other invertebrates, including actinians (Chace, 1958, 1972; Mahnken, 1972; Sargent and Wagenbach, 1975; Herrnkind, Stanton, and Conklin, 1976), scyphozoans (Bruce, 1972a), zoantharians (Bruce, 1973), antipatharians (Davis and Cohen, 1968), anthozoans (Bruce, 1972b), echinoids (Bruce, 1972c; Castro, 1974), and molluscs (Shoup, 1972; Bruce, 1975). In the shrimp genus Periclimenes some species associate with sea anemones while others, in addition to living with sea anemones, are cleaning symbionts of reef fishes (Chace, 1958; Limbaugh, Pederson, and Chace, 1961; Feder, 1966; Mahnken, 1972; Sargent and Wagenbach, 1975). Several of these invertebrate hosts, most notably sea anem- Ones, possess stinging nematocysts that are utilized in prey capture, but their shrimp symbionts are apparently not affected by them (Feder, 1966; Mahnken, 1972; Herrnkind et al. 1976). It is clear that the exoskeleton of the shrimps per se do not protect them from the nematocysts of sea anemones. We have seen non-commensal crustaceans stung by the sea anemone Stoichactis helianthus (Ellis), and Herrnkind et al. (1976) observed that large non-commensal crustaceans were stung by the sea anemone Lebrunia danae (Duchassaing and Michelotti). A similar symbiotic relationship exists between certain pomacentrid fishes and sea anemones (Mariscal, 1972; Allen, 1975). Early workers who studied the po- macentrid fish-anemone symbiosis discovered that the fish became vulnerable to the nematocysts after a period of isolation from their host and had to undergo a behavioral process known as acclimation (Davenport and Norris, 1958; Mariscal, 1965, 1966, 1969, 1970a, 1970c, 1971; Schlichter, 1967, 1968). These workers concluded that a change occurred in the mucus coat of the fish that provided protection from the nematocysts. Schlichter (1970, 1972) performed a series of experiments in which he used sea anemones labeled with tritiated amino acids. The tritiated label was taken up by the sea anemones and accumulated in the surface mucus of the tentacles. Previously isolated anemonefishes were then al- lowed to acclimate to the anemones. Through the use of autoradiographic tech- nique, Schlichter (1972) found that the tritiated label was transferred onto the surface of the fish during acclimation. The highest concentrations of the label were found in those areas which most frequently contacted the tentacles. Schli- chter (1972) concluded that the fish were "chemically camouflaged" as a result of incorporating the anemone mucus into their mucus coat. It is not known wheth- er the anemone mucus forms a complex with the mucus coat of the fish or whether it masks it in some way. 460 LEVINE AND BLANCHARD: ACCLIMATION OF SHRIMPS TO SEA ANEMONES 461 Table I. Results of isolation experiments for Periclimenes rathbllnae and its anemone host, Sto- ichactis helianthlls Anemone Anemone Without With Total No. of Shrimp Shrimp Shrimp Observ~tions Summary of Results U naccl imated Unacclimated + + (10) (10) 20 shrimps stung Acclimated Acclimated (10) (6) 16 shrimps not stung Total no. of observations 20 16 36 Numbers in parentheses refer to number of experiments + = shrimp slung; - = shrimp not stung. The purpose of this study was to determine through a series of laboratory behavioral experiments the protective mechanisms involved in the symbioses between the shrimp Periclimenes rathbunae Schmitt and the sea anemone Sto- ichactis helianthus (Ellis), and the shrimp Periclimenes anthophilus Hothuis and Eibl-Eibesfeldt and the sea anemone Condylactis gigantea (Weinland). The ex- perimental design was patterned after Mariscal (1969, 1970a, 1971) in studying the pomacentrid fish-anemone symbiosis. Reciprocal experiments were conduct- ed in which both acclimated and unacclimated shrimps were tested against anem- ones with and without (acclimated and unacclimated, respectively) shrimps living with them. The rationale behind these experiments was as follows: if only un- acclimated shrimps were stung by sea anemones, both with and without shrimps, this would indicate that some change had occurred in the shrimps during accli- mation which resulted in their protection. Conversely, if only the sea anemones containing acclimated shrimps failed to sting shrimps (either acclimated or un- acclimated), this would indicate that some change had occurred in the sea anem- one during acclimation, which resulted in the shrimp's protection (Mariscal, 1969, 1970a, 1971). METHODS AND MATERIALS Periclime/les rathbll/lae shrimps and S. helia/lthlls anemones were collected from Innes Bay, Port- land Parish, Jamaica, during December 1976, and transported to Earlham College, Richmond, Indiana where laboratory experiments were conducted in all-glass aquariums containing Instant Ocean brand synthetic sea water. Periclime/les a/lthophillis shrimps and C. giga/ltea anemones were collected during June and July 1978, from Whalebone Bay, Shelly Bay, Castle Harbor, John Smith's Bay, Harrington Sound, Baily's Bay, and North Rock, Bermuda. Laboratory observations were made on animals held in running sea water aquariums at the Bermuda Biological Station for Research. Sixty hours of field observations were made in Jamaica with the aid of snorkeling gear, and 16 h in Bermuda with the aid of SCUBA and snorkeling gear. Observations were made on the four experimental conditions mentioned above. Reciprocal exper- iments were conducted in which both acclimated and unacclimated shrimps were tested against their host sea anemone species with and without shrimp living with them (acclimated and unacclimated anemones, respectively). An acclimated shrimp was defined as a shrimp living with a sea anemone at the time of an experiment, and an unacclimated shrimp as one which had been isolated from anemones for 24 h. Shrimps were observed every 0.5 h for 5 minutes to determine if acclimation was complete. Criteria similar to those of Mariscal (1969, 1970a, 1971) were used to determine whether a shrimp was stung during experiments. The criteria were: strong tentacle adhesion to the legs, tail, and abdomen, a quick sudden jump backwards off the oral disc of the anemone when initially contacting the tentacles, and strong contraction of the anemone in response to the presence of the shrimp. The term "stung" is defined here as the action of spirocysts and nematocysts adhering to the exoskeleton that would result in the shrimp's capture if escape is not effected. Mariscal's (1969, 1970a, 1971) criteria for testing the anemones prior to each experiment were used to insure that they were capable of prey capture. These criteria included presenting live prey to the anemones, passing a finger through 462 BULLETIN OF MARINE SCIENCE. VOL. 30, NO.2, 1980 Table 2. Results of isolation experiments for Periclimenes anthophilus and its anemone host, Con- dy/actis gigantea Anemone Anemone Without With Total No. of Shrimp Shrimp Shrimp Observations Summary of Results Unacclimated Unacclimated + + (8) (20) 28 shrimps stung Acclimated Acclimated (10) (22) 32 shrimps not stung Total no. of observations 18 42 60 Numbers in parentheses refer to number of experiments + = shrimp stung; - = shrimp not stung. the tentacles, which always resulted in strong adhesion, and passing gelatin-coated slides through the tentacles. The slides were examined microscopically for basitrichous isorhiza nematocysts. The shrimps were captured and transferred between aquaria using pyrex beakers. They were never taken out of sea water. Mariscal (1970a) found no difference in the results when fish or anemones were transferred. and therefore anemones were usually left in their aquaria and the shrimps were trans- ferred. Holthuis and Eibl-Eibesfeldt (1964) reported P. (/nthophilus in association with the anemone Actinia bermudensis McMurrich in Whalebone Bay, Bermuda. After preliminary field observations that did not concur with this report, a laboratory experiment was conducted to determine whether P. uwho- philus would associate with Actinia. Ten anemones and shrimps were placed in 11 cm diameter finger bowls, and observed every 0.5 h for 4 h. RESULTS AND DISCUSSION Periclimenes rathbunae shrimps and S. helianthus anemones were found in the field at depths ranging from 0.3 to 3.0 m. One or two shrimps were found on a single anemone. Periclimenes anthophilus shrimps and C. gigantea anemones were found in the field at depths ranging from 1 to 15 m. The number of these shrimps on a single anemone varied from 2 to 11 individuals. Both species of shrimp were always found among the tentacles of their respective hosts, and the tentacles never reacted to the presence of the shrimps. The results of the isolation experiments
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