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Asexual Reproduction by the Symbiotic Sea Anemone <I>Calliactis Tricolor

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Asexual Reproduction by the Symbiotic Sea Anemone <I>Calliactis Tricolor BULLETIN OF MARINE SCIENCE, 36(3): 432-435,1985 ASEXUAL REPRODUCTION BY THE SYMBIOTIC SEA ANEMONE CALLIACTIS TRICOLOR (LESUEUR) William R. Brooks and Richard N. Mariscal ABSTRACT Previously, it was unknown how the symbiotic sea anemone Calliactis tricolor reproduced. The present paper reports the discovery of a C. tricolor anemone that was undergoing lon- gitudinal fission. Other anemones were also collected that had the distinctive column scars characteristic of recently separated anemones. These observations represent the first direct evidence for any type of reproduction by C. tricolor. In addition, small C. tricolor were found at one locality. These small anemones could have been produced sexually. Sea anemones can reproduce sexually, asexually, or both (for a review, see Chia, 1976). As in most organisms, an anemone's reproductive mode can affect its distribution and abundance (Francis, 1973; Shick and Lamb, 1977; Dunn, 1982; Ayre, 1983). Because of their world-wide distribution and interesting behavior, the associ- ation of sea anemones, especially those belonging to the genus Calliactis, with crabs has been of long-standing interest to workers from a variety of biological disciplines (Ross, 1974). In spite of the many behavioral studies of this classic example of symbiosis, reproduction by Calliactis has only been reported by a few workers. Faurot (1895) and Stephenson (1935) have both reported that C. par- asitica reproduces sexually. Faurot (1895) stated that C. parasitica is viviparous, but Stephenson (1935) stated that it is oviparous. In addition, Cutress (pers. comm.) reported spawning and rearing C. polypus planulae for up to 36 days. Several workers have also reported finding young Calliactis associated with crabs, which indirectly suggests that sexual reproduction occurs. Cutress et at. (1970) have collected what they call "very small" C. tricolor on a Caribbean spider crab, Stenocionops jurcata. In addition, Ross (1980) reports that many C. par- asitica with pedal disc diameters of less than 2 mm were found on the Mediter- ranean hermit crab Paguristes oculatus. The discovery of small anemones suggests that they have recently settled after undergoing metamorphosis from planktonic larvae, presumably as a result of sexual reproduction. Although sexual reproduction in certain Calliactis sp. has been observed, neither sexual nor asexual reproduction has been reported for C. tricolor. In the present study, we provide evidence for the first time of asexual reproduction by longi- tudinal fission in the sea anemone Calliactis tricolor. MATERIALS AND METHODS The anemone Calliactis tricolor (Lesueur) was collected during November 1983, on gastropod shells that were inhabited by the hermit crab Pagurus pollicaris Say at two intertidal sites in the northeastern Gulf of Mexico. One locality was near the Florida State University Marine Laboratory (FSUML), located at Turkey Point, Florida, about 45 miles south of Tallahassee. The second locality was in St. Joseph Bay, adjacent to Port St. Joe, Florida, and about 50 miles west of the FSUML. Collections were made in 1-2 m of water by either snorkeling or wading. The pedal disc diameter of each Calliactis was measured while the anemone was on the gastropod shell. If the attached portion of the anemone's pedal disc was irregularly shaped (non-circular), then two measurements of the widest and narrowest dimensions were averaged (Ross, 1980). Anemones were maintained either singly or together, de- pending on their reproductive state, and fed freshly hatched Artemia nauplii every 3 to 4 days. 432 BROOKS AND MARISCAL: REPRODUCTION OF CALLIACTIS 433 CD Figure I. The anemone Calliactis tricolor as it appeared on the gastropod shell when collected. Nolice that the anemone is undergoing longitudinal fission. Figure 2. One week later, the anemone has separated into two functional individuals. Figure 3. One anemone subsequently moved off the original shell, crawled along the substratum, and then, 2 days later, climbed onto another shell that had a hydroid colony on it. Notice the opaque areas on the columns of the two clones (as indicated by the arrows). Figure 4. One of several Cal/iactis collected that had an opaque area on its column, similar to the areas seen on the two clones in the previous picture. RESULTS A P. pollicaris hermit crab in a Polinices duplicatus (Say) shell that appeared to have two anemones on it was collected near the FSUML. Upon closer inspec- tion, it was evident that only one anemone was present. This anemone, however, appeared to be undergoing longitudinal fission (Fig. I) (for a recent review of asexual reproduction by sea anemones, see Chia, 1976). The anemone was taken back to the lab, and 1 week later longitudinal fission was completed, resulting in two Calliactis on the single shell (Fig. 2). Subsequently, one individual moved off the original shell onto another P. duplicatus shell, which was covered by the hydroid Hydractinia echinata (Fleming) (Fig. 3). Although no other anemones were found undergoing longitudinal fission, three other anemones were also collected near the FSUML that had light-colored, 434 BULLETIN OF MARINE SCIENCE, VOL. 36, NO.3, 1985 Table I. The average pedal disc diameters of Ca/liactis tricolor collected from two locations in north Florida are compared using Wilcoxon's Rank Sum test. The anemone that was undergoing asexual reproduction was not included in the calculation of the mean for the anemones from the Florida State University Marine Lab (FSUML) Collection site FSUML SI. Joseph Bay Number individuals 9 13 Mean pedal disc diameter (mm) 20.0 5.5 SD 4.8 2.6 Range (mm) 12-27 2-10 P < 0.0001 opaque scars on their columns that were similar to areas on the columns of the two anemones that had just undergone longitudinal fission (Fig. 4). Ten of 45 P. pollicaris hermit crabs that were collected near the FSUML each had one C. tricolor on its shell (one of which was undergoing longitudinal fission as described above). The average pedal disc diameter for this group was 20.0 mm. Thirteen of 75 P. pollicaris that were collected in St. Joseph Bay each had one C. tricolor on its shell, none of which appeared to be undergoing longitudinal fission. The average pedal disc diameter for this latter group was 5.5 mm (Table 1). The anemones from S1. Joseph Bay were much smaller than those from near the FSUML, with three having pedal disc diameters of only 2 mm. The average pedal disc diameters of the two groups of anemones were significantly different (Table 1). DISCUSSION This study presents direct evidence for the first time showing that Calliactis reproduces asexually. One anemone was observed undergoing longitudinal fission and subsequently separated into two individuals. In addition, the light-colored scars on the columns of two additional anemones collected indicated that they had also recently divided. Both Walton (1918) and Sebens (1983) observed similar scars on other anemones. Walton (1918), while studying longitudinal fission by the anemone Actinia bermudensis, observed opaque areas on recently separated anemones, describing them as " ... salmon-pink tissue, 3-5 mm wide, and running the whole length of the column." Similarly, Sebens (1983) observed white division scars on Anthopleura elegantissima that had recently undergone longitudinal fis- SIOn. It is not known at this time how often C. tricolor reproduces asexually. Ap- parently, it is very infrequent because Cutress (pers. comm.) has observed many Calliactis internally and all have been the most regular anemones he has ever seen. They all had two directive mesenteries, two siphonoglyphs, and six pairs of perfect septa. If longitudinal fission were common in Calliactis, irregular anem- ones should also be common. The discovery in the present study of small C. tricolor suggests that sexual reproduction in this species may also occur. Because sexual reproduction has been observed in the closely related C. polypus (Cutress, pers. comm.), it is quite likely that C. tricolor also reproduces sexually. The discovery of asexual reproduction by longitudinal fission in C. tricolor adds to our understanding of symbiotic associations between sea anemones and hermit BROOKS AND MARISCAL: REPRODUCfION OF CALLIACTlS 435 crabs. Further studies are needed, however, to determine the complete life histories of these anemones in relation to their crab hosts. ACKNOWLEDGMENTS We would like to thank P. G. Greenwood for suggestions and criticism of the manuscript. Special thanks go to Dr. C Cutress who reviewed this manuscript and who also allowed us to use his unpublished observations. We would also like to thank Florida State University for financial support in the form of a University Fellowship to the senior author. This is contribution No. 1006 of the Florida State University Marine Laboratory, Turkey Point, Florida. LITERATURE CITED Ayre, D. J. 1983. The effects of asexual reproduction and intergenotypic aggression on the genotypic structure of populations of the sea anemone Actinia tenebrosa. Oecologia 57: 158-165. Chia, F. S. 1976. Sea anemone reproduction: patterns and adaptive radiation. Pages 261-270 in G. O. Mackie, ed. Coelenterate ecology and behavior. Plenum Press, New York. Cutress, C, D. M. Ross and L. Sutton. 1970. The association of Calliactis tricolor with its pagurid, calappid, and majid partners in the Caribbean. Can. J. Zool. 48: 371-376. Dunn, D. F. 1982. Sexual reproduction of two intertidal sea anemones (Coelenterata: Actiniaria) in Malaysia. Biotropica 14: 262-27 I. Faurot, L. 1895. Etudes sur I-anatomie, I-histologie, et Ie developpement des Actinies. Arch. Cool. Exp. Gen., Paris, (3)3: 43-262, pis. 1-12. Francis, L. 1973. Clone specific segregation in the Anthopleura elegantissima. BioI. Bull. 144: 64-72. Ross, D. M. 1974. Evolutionary aspects of associations between crabs and sea anemones. Pages 111-125 in W. B. Vernberg, ed. Symbiosis in the sea. University of South Carolina Press, Co- lumbia, South Carolina. ---. 1980. Post-metamorphic life history of the symbiotic anemone Calliactis parasitica (Couch).
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