Gregariousness in the Gorgonian-Eating Gastropod Cyphoma Gibbosum:Tests of Several Possible Causes
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MARINE ECOLOGY - PROGRESS SERIES Vol. 31: 255-263. 1986 Published July 24 Mar. Ecol. Prog. Ser. Gregariousness in the gorgonian-eating gastropod Cyphoma gibbosum:tests of several possible causes Donald J. Gerhart* Department of Ecology and Evolution. SUNY at Stony Brook. Stony Brook, New York 11794, USA ABSTRACT: The ovulid gastropod Cyphorna gibbosum IS a widespread and common predator of gorgonian octocorals ('sea whips') on Caribbean coral reefs. C. gibbosum is not randomly distributed, but tends to be clumped into small groups. To examine possible causes of this phenomenon, field and laboratory experiments were performed with C. gibbosum and Plexaura hornornalla, a common Caribbean gorgonian. These experiments suggest that clumping in C. gibbosum is produced by mucous trail following. Gregariousness may have evolved in C. gibbosum to increase the protection afforded by distastefulness and aposematism, although other explanations cannot be excluded. Octocoral-gastropod interactions possess several important parallels to terrestrial plant-herbivore systen~s.Further comparison of these systems may provide new insights into predator-prey coevolution. INTRODUCTION throughout the Caribbean (Ghiselin & Wilson 1966, Kinzie 1971), feeds exclusively on gorgonians. Gorgonians (Coelenterata: Anthozoa: Octocorallia) Kinzie (1971) concluded that Cyphoma gjbbosum are common, conspicuous members of Caribbean coral was a generalist within the order Gorgonacea, with no reef communities. In spite of their conspicuousness, inter-specific prey preferences. Other studies suggest gorgonians are rarely eaten by predators (Randall that Cyphoma gibbosum favors certain species of gor- 1967, Vermeij 1978, Bakus 1981). This observation is gonians (Birkeland & Gregory 1975). For any given intriguing, since predation on coral reefs is intense prey species, however, individual Cyphoma gibbosurn (Glynn et al. 1972, Bakus 1964, 1971, 1981, Sammarco are not distributed randomly, but tend to be clumped et al. 1974, Brock 1979, Sammarco 1980, Huston 1985). into small groups (Birkeland & Gregory 1975, Hazlett & Gorgonians possess several lines of defense against Bach 1982). The most dramatic examples of clumping predators, including sclerites of calcium carbonate are those reported by Kinzie (1971) of a group of 17 C. (Bayer 1961),nematocysts (Barnes 1980, Hyman 1940), gibbosurn grazing on a single gorgonian colony, and and large amounts of secondary compounds (Tursch et the observations of Birkeland & Gregory (1975) of al. 1978, Fenical 1982, Faulkner 1984). Since predation aggregations of 16, 28, and 35 individuals. can play an important role in the structuring of ecologi- Hazlett & Bach (1982) found that the clumped dis- cal communities (Slobodkin 1962, Paine 1966), these tribution of Cyphoma gibbosum was not explained by defenses may significantly affect the patterns of dis- colony size, or by the distance to the nearest neighbor- tribution and abundance of gorgonians. ing gorgonian colony. These authors contended that A few organisms have circumvented the defenses of clumping could be produced by intercolony variation gorgonians. Perhaps the most notable of these is in the quahty of the gorgonians, as perceived by the Cyphoma gibbosum, a gastropod in the family snails. Hazlett & Bach suggested that these differences Ovulidae. This snail, which is common on coral reefs in prey quality could be the result of intraspecific variation in the secondary metabolite content of gorgo- Present address: Department of Chemistry, 2545 The Mall, nians. University of Hawaii at Manoa. Honolulu, Hawaii 96822. USA Variation in secondary metabolite content is well O Inter-Research/Printed in F. R. Germany 256 Mar. Ecol. Prog. Ser. 31: 255-263, 1986 documented in Plexaura homornda, an abundant gor- are toxic or noxious (Tursch et al. 1978, Bakus 1981), C. gonian on shallow Caribbean coral reefs. A single gibbosurn also may be distasteful. If so, then gregari- chemical compound, prostaglandin A? (PGA2), com- ousness in this snail may lead to decreased susceptibil- prises 2 to 8% of the wet weight of P. homomalla ity to predation. (Weinheimer & Spraggins 1969, Schneider et al. 1977, To test these hypotheses, I performed a series of field Dominguez et al. 1980). Prostaglandins are fatty-acid and laboratory experiments at Curaqao, Netherlands derivatives with potent, hormone-like effects on a wide Anhlles, where Plexaura homomalla reportedly con- range of biological processes (Hall & Behrman 1982). tained a mixture of 15(R)- and 15(S)-PGA2(Schneider PGA2 appears to provide P. homomalla with an effec- & Morge 1971). The objectives of these experiments tive defense against predatory fish (Gerhart 1984a, b). were: (l)to document the distribution of Cyphoma In spite of the large amount of PGA2 in its tissues, gibbosum on colonies of Plexaura homomalla; (2) to however, P, homornalla is readily consumed by determine if snail-grazed colonies of P. homomalla Cyphoma gibbosum (Kinzie 1971, Gerhart 198413). differed significantly from ungrazed colonles in their The prostaglandin content of Plexaura homomalla size, population density, proximity to other gorgo- varies from location to location within the Caribbean nians, or prostaglandin isomer content; (3) to deter- (Schneider & Morge 1971, Schneider et al. 1977, mine if colonies of P. homomalla that were previously Gerhart 1984b). In some areas, colonies contain 15(S)- chosen by C. gibbosum were more acceptable to the PGA2, while in other locations, P. homomalla contains snails than colonies that had not been chosen; (4) to mostly the 15(R) isomer of PGA,. In several mamma- determine whether individuals of C. gibbosum lian bioassays, 15(S)-PGA2 is highly potent, while attracted others as they grazed on their gorgonian 15(R)-PGA2 possesses little or no activity (Nakano prey; (5) to elucidate the role of mucous trail following 1968, 1969, Nakano & Kessinger 1970, Spraggins in the production of the clumped distribution of C. 1972). If the activity differences of 15(R)- and 15(S)- gibbosum; (6)to determine whether C. gibbosum was PGA2 in Cyphoma gibbosum parallel those observed unpalatable to predators. in mammals, then C. gibbosum may prefer colonies of Plexaura homomalla which contain the less potent 15(R) isomer of PGA2. MATERIALS AND METHODS Thus, the clumped distribution of Cyphorna gib- bosum may occur because some prey colonies are more The study was performed at Kaap Malmeeuw and at acceptable to the snails than others. If so, then snails CARMABI Buoy Two on the southwest coast of transplanted to gorgonian colonies that were previ- Curaqao. These locations have been described by Van ously occupied by C. gibbosum should remain longer, den Hoek et al. (1978). on average, than snads moved to previously vacant Intercolony distribution of Cyphoma gibbosum. Fifty colonies. Furthermore, if differences in the acceptabil- colonies of Plexaura homornalla were selected ity of colonies are caused by variation in secondary haphazardly and marked with numbered plastic tags. metabolite content, this variation should be demon- Tags were tied to a nearby piece of dead coral to strable by chemical analysis of the tissue. reduce disturbance of the gorgonian. The colonies Alternatively, snails may choose colonies at random, were examined 4 to 5 times wk-l, from September 13 and subsequently attract other snails to the occupied through November 7, 1983. Five additional colonies of colony. If this is true, then Cyphoma gibbosum trans- P. homomalla, each occupied by at least 2 snds, were planted to previously vacant colonies should remain as added to the study on September 27, 1983. All observa- long, on average, as those moved to previously tions were made using SCUBA. occupied colonies. Furthermore, consistent chemical The following data were taken for each numbered differences between occupied and vacant colonies colony: (l)the distance to the nearest neighboring should not be found, and snarl-occupied gorgonians gorgonian; (2) the distance to the nearest neighboring should be chosen more frequently than unoccupied colony of Plexaura homomalla; (3) the distance to near- gorgonian colonies. est gorgonian colony occupied by a snail; (4) the max- The latter hypothesis presumes that snails have, for imum height of the colony. Tissue samples were col- some unknown reason, evolved gregarious behavior. lected from each colony at the end of the study and In terrestrial insects, gregariousness is frequently later analyzed by high efficiency thin-layer associated with distastefulness, presumably to better chromatography (HETLC) to determine the 15(R)- and exploit the defensive benefits of unpalatability (Fisher 15(S)-PGA2content of the tissue (Schneider & Morge 1958). Cyphoma gibbosum appears to sequester secon- 1971, Schneider et al. 1977, Gerhart 1984b). dary chemicals from its gorgonian prey (Steudler et al. Transplant experiments with Cyphoma gibbosurn. 1977). Since many gorgonian secondary compounds During the months of October and November 1984, 54 Cerhart: Gregariousness in a gorgonian-eating gastropod 257 colonies of Plexaura homomalla were tagged at CAR- the second run and after each subsequent run. To make MABI Buoy Two. Of these colonies, 22 were occupied sure that the snails were not influenced by differences by Cyphoma gibbosum, and the remainder were va- in the gorgonian branches, the branches were cant. At the beginning of the experiment, all snails switched between Runs 3 and 4. Finally, to ensure that were removed from the occupied colonies.