NOTES

BULLETIN OF MARINE SCIENCE, 39(1): 130-134, 1986

BEHAVIORAL ASSOCIAnONS OF CORAL REEF FISHES WITH THE SEA ANEMONE CONDYLACTIS GIGANTEA IN THE DRY TORTUGAS, FLORIDA

Roger T. Hanlon and Raymond F. Hixon

Over 30 small West Indian reef fishes dwell within the tentacular sphere of anemones, mainly to avoid predation (Colin and Heiser, 1973; Smith, 1973; Hanlon and Kaufman, 1976; Albrecht, 1977; Stanton, 1977; Hanlon et al., 1983). Most species swim carefully to avoid the stinging tentacles, but some species (Hanlon et al., 1983) also have a physiological adaptation (skin mucus alteration) that allows them to be in full and vigorous contact with the tentacles in a manner similar to Indo-Pacific anemonefishes such as Amphiprion, Dascyllus and Premnas (Allen, 1975). We report herein six species of reef fishes that are facultative associates of the sea anemone Condylactis gigantea (Weinland) in the Dry Tor- tugas Islands (24°38'N, 82°55'W). The fishes were not found associated with other anemones. One species, Labrisomus gobio, is a new record of a fish with both the behavioral and physiological adaptations to dwell unharmed among the stinging tentacles of Condylactis gigantea,

METHODS

All observations, photographs and collections were made underwater during day and night snorkel and SCUBA dives (total 35) between 31 May and 16 June 1983, In all cases, anemones were observed intensively and carefully (up to 30 min) to ascertain if fishes were inhabiting anemones; photographs and behavioral notes were taken during observations. Most anemones and their fish associates were observed several times throughout the observation period. Only after observation were collections made by squirting a 10% quinaldine-alcohol anaesthetic solution into the tentacular sphere and netting the observed fish. Collected fishes were photographed alive aboard ship at the collecting sites before being preserved in 10% formalin. Specimens are deposited in the fish collection of the Rosenstiel School of Marine and Atmospheric Science, University of Miami (UMML), Florida 33149. We recognize the Labrisomidae (George and Springer, 1980; Matarese et al., 1984) as a family rather than a subfamily of the Clinidae. Common names are in accordance with Bailey et al. (1980).

OBSERVATIONS Labrisomidae. -Labrisomus gobio (Valenciennes). One palehead blenny was col- lected: immature female, 60 mm standard length (SL) (UMML 34321),3 m deep on a patch reef immediately west ofthe middle of Loggerhead Key. This fish was observed on a dawn dive (approximately 20 min before the diurnal turnover) sitting on the oral disc ofthe anemone and completely covered by tentacles (Fig. lA, B). It moved within, under and around the anemone with no unusual reactions and without eliciting nematocyst discharge or retraction by the tentacles. The fish moved away from the anemone voluntarily after 20 min of observation, and this coincided with the first movement of many other fishes that had been sleeping or hiding during the night and were moving up and onto the reef. One other L. gobio was observed in Condylactis during the day, but it was not collected. The live coloration was very similar to that described by Bohlke and Chaplin (1968).

130 NOTES 131

Figure 1. Fishes in full contact with the tentacles of the sea anemone Condylactis gigantea in the Dry Tortugas. A. Typical arrangement of two anemones on the patch reefs immediately adjacent to Loggerhead Key. Both anemones had fishes in them-Labrisomus gobio in the left anemone, Mala- coctenus triangulatus in the right one. 3 m deep. B. An immature female palehead blenny, Labrisomus gobio. 60 mm SL, sitting on the tentacles of the left anemone in (A) just before dawn. C. The saddled blenny, Malacoctenus triangulatus. sitting at the base of the right anemone in (A) just before dawn. D. An immature M. triangulatus. 49 mm SL, hiding amidst the tentacles at night on a patch reef, 5 m deep, on the NE tip of Loggerhead Key.

To our knowledge this is the first record of L. gobio from the Tortugas, although it occurs nearby at Cay Sal Banks (Bahamas) and Cuba (Bohlke and Chaplin, 1968). Labrisomus kalisherae (Jordan). One downy blenny was collected: immature female, 53 mm SL (UMML 34320), 5 m deep on a patch reef approximately 30 m off the NE tip of Loggerhead Key. This fish was collected at dusk and was fully in contact with the tentacles of Condylactis gigantea in the manner described for L. gobio. This species was observed by Smith (1973) to dwell for 2 months unharmed within a Condylactis gigantea off Panama. No other fishes of this species were observed, although Longley (1941) mentions this species as common in the Tortugas. Malacoctenus triangulatus Springer. Three saddled blennies were collected from anemones: (1) an immature specimen, 14 mm SL (UMML 34317), that was touching the tentacles with no apparent harm, on a very small and isolated patch reef in a seagrass bed 7 m deep NE of East Key during the day; (2) an immature specimen, 49 mm SL (UMML 34318), that was covered by tentacles while sitting on the oral disc at night (Fig. ID) 5 m deep on the same patch reef as Labrisomus 132 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.1, 1986 kalisherae; and (3) a female, 46 mm SL (UMML 34319), that was also covered by tentacles at night in an anemone only 0.5 m away from the anemone in which specimen 2 (above) was collected. This was the most common blenny we observed in the Tortugas: three others were observed in Condylactis but not collected and seven others were observed on the same reefs but not in association with anem- ones. All were found in shallow water (1-5 m) on reefs except one, which was on a spur and groove reef at 15 m. Malacoctenus triangulatus has been described as associating with Condylactis in Jamaica by Hanlon and Kaufman (1976), and its occurrence in the Tortugas has been documented by Springer (1958). This species was most conspicuous on the reef because its behavior was less cryptic than other blennioid fishes and its pattern of triangles was relatively bold. Mature males of M. triangulatus in a reproductive state have a very bright and conspicuous coloration in which the entire head and the inverted triangles on the body are nearly black, while the rest of the body, including most or all ofthe fins, is light to moderately deep orange. This is strikingly different from the typical coloration in males or females as described in Bohlke and Chaplin (1968) or any of the color morph variations cited in Springer and Gomon (1975). Males and females both occasionally display splotches of orange or red coloration ventrally and on the fins, but the sharp sexual dichromatism we observed seems to be specific to reproductive males. Seven such males were observed, four were pho- tographed underwater and one was collected (mature male, 42 mm SL, UMML 34316); the collected male lost all orange coloration when preserved. One ofthese males (uncollected) was photographed sitting among the tentacles of Condylactis at night. On two occasions, pairs of M. triangulatus (one bright orange, the other normal) showed presumed courtship behavior in which the orange fish (presumed male) flapped its gill covers to its sitting partner, then swam swiftly up into the water column with fast gyrations, then sat next to the sitting partner (presumed female) and nuzzled up to it for 5 sec. The fishes then parted. None of these four fishes were collected, so sex and reproductive state could not be verified. At no other time were any blennies seen in pairs. Malacoctenus macropus (Poey). No collections. One rosy blenny was observed in midday nestled amidst the tentacles of Condylactis on an isolated patch reef surrounded by seagrass on the east side of Loggerhead Key in 3 m of water. All interactions were similar to those reported earlier (Hanlon and Kaufman, 1976). Labridae. - Thalassoma bifasciatum Bloch. No collections. One juvenile bluehead wrasse was seen near the oral disc (5 m deep) and avoiding tentacles as described by Hanlon and Kaufman (1976). Scaridae. - One juvenile parrotfish was observed swimming within the tentacular sphere and against the oral disc of an anemone (3 m deep), but avoiding the tentacles in a manner described previously (Hanlon et aI., 1983).

DISCUSSION Nine Caribbean reef fishes are now known to have the behavioral and phys- iological adaptations for dwelling unharmed within the tentacles of the sea anem- one Condylactis gigantea: Labrisomus gobio (this report), L. haitiensis, L. kalishe- rae, Malacoctenus boehlkei, M. gilli, M. macropus, M. triangulatus, Starksia hassi and Paraclinus grandicomis (Bohlke and Chaplin, 1968; Smith, 1973; Hanlon and Kaufman, 1976; Herrnkind et aI., 1976; Stanton, 1977; Hanlon et aI., 1983). It was demonstrated in Malacoctenus that the fishes are stung during acclimation, which took from several minutes to several hours (Hanlon and Kaufman, 1976). NOTES 133

These associations all appear to be facultative since the same species are commonly not associated with anemones in the same locales. No obligate associations are known in the Caribbean. While over 30 Caribbean reef fishes sometimes inhabit sea anemones (Hanlon and Kaufman, 1976; Albrecht, 1977), it is significant that the species with some measure of protection from stinging are in the family Labrisomidae. Four of the eight Caribbean species of Malacoctenus are confirmed anemone dwellers, three of nine Labrisomus, one of eight Paraclinus and one of 15 Starksia. Another related blennioid fish, Emblemariopsis diaphana Longley (Family Chaenopsidae), has been reported as dwelling unharmed in another ac- tinian, the stony coral Meandrina meandrites (Butter et al., 1980). With further careful observations underwater, it will not be surprising to find other blennioid fishes with special adaptations to actinians, which are so prevalent in the coral reef habitat. Recent experimental work on the mechanism of acclimation to anemones by Pacific anemonefishes (Brooks and Mariscal, 1984) supports the hypothesis that the fish alters its own mucous coating to avoid stinging (Lubbock, 1979; 1980) and does not acquire anemone mucus during acclimation to avoid being stung by the anemone (Schlichter, 1976). Comparative work on symbionts of Condy- lactis such as fishes of the family Labrisomidae or shrimps of the genera Thor or Periclymenes (Levine and Blanchard, 1980) may be useful in elucidating this physiological adaptation.

ACKNOWLEDGEMENTS

This work is dedicated to Dr. Raymond F. Hixon, a great friend, trusted diving companion, keen underwater observer and fellow biologist who died in 1984 from complications after a bone marrow transplant for leukemia. We thank Drs. D. G. Smith and C. R. Robins for aid in fish identification, and the National Park Service for permission to work in the Tortugas. Financial support was gratefully received from the Marine Medicine account of The Marine Biomedical Institute, The University of Texas Medical Branch.

LITERATURE CITED Albrecht, H. 1977. Einige Beobachtungen an Anemonenfischen in der Karibischen See. Bijdragen tot de Dierkunde 47: 109-119. Allen, G. R. 1975. The anemonefishes, 2nd ed. T.F.H. Publications, Neptune City. 352 pp. Bailey, R. M., 1. E. Fitch, E. S. Herald, E. A. Lachner, C. C. Lindsey, C. R. Robins and W. B. Scott. 1980. A list of common and scientific names of fishes from the United States and Canada. Amer. Fish. Soc., Spec. Pub. No.6., 2nd Ed. American Fisheries Society, Bethesda. 150 pp. Bohlke, J. E. and C. C. G. Chaplin. 1968. Fishes of the Bahamas and adjacent tropical waters. The Academy of Natural Sciences of Philadelphia. Livingston Publishing Co., Wynnewood, Pa. 771 pp. Brooks, W. R. and R. N. Mariscal. 1984. The acclimation of anemone fishes to sea anemones: protection by changes in the fish's mucous coat. J. Exp. Mar. BioI. Ecol. 81: 277-285. Butter, M. E., M. Wapstra and E. V. Dijk. 1980. Meandrina meandrites and Emblemariopsis di- aphana, first record of an association between a stony coral and a fish, similar to anemone fish relationships. Bijdragen tot de Dierkunde 50: 87-95. Colin, P. L. and J. B. Heiser. 1973. Associations of two species of cardinalfishes (Apogonidae: Pisces) with sea anemones in the West Indies. Bull. Mar. Sci. 23: 521-524. George, A. and V. G. Springer. 1980. Revision of the Clinid fish tribe Ophiclinini, including five new species, and definition of the Family Clinidae. Smithson. Contr. Zool. (307). 31 pp. Hanlon, R. T. and L. Kaufman. 1976. Associations of seven West Indian reef fishes with sea anemones. Bull. Mar. Sci. 26: 225-232. --, R. F. Hixon and D. G. Smith. 1983. Behavioral associations of seven West Indian reef fishes with sea anemones at Bonaire, Netherlands Antilles. Bull. Mar. Sci. 33; 928-934. Hermkind, W., G. Stanton and E. Conklin. 1976. Initial characterization of the commensal complex associated with the anemone, Lebrunia danae. at Grand Bahama. Bull. Mar. Sci. 26: 65-71. 134 BULLETINOFMARINESCIENCE,VOL.39, NO,1. 1986

Levine, D. M, and O. J. Blanchard, Jr. 1980. Acclimation of two shrimps of the genus Periclimenes to sea anemones. Bull. Mar. Sci. 30: 460-466. Longley, W. H. 1941. Systematic catalogue of the fishes of Tortugas, Florida. With observations on color, habits, and local distribution. Carnegie Instit. Wash. Publ. 535, 2: 172-331. Lubbock, R. 1979. Chemical recognition and nematocyte excitation in a sea anemone. J. Exp. BioI. 83: 289-292. --. 1980. Why are clownfishes not stung by sea anemones? Proc. Roy. Soc., Lond. 207B: 35-61. Matarese, A. c., W. Watson, and E. G. Stevens. 1984. Blennioidea: development and relationships. Pages 565-573 in H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. Kendall, Jr. and S. L. Richardson, eds. Ontogeny and systematics of fishes. Special Publ. No. I, Amer. Soc. Ichthy. and Herp. Schlichter, D. 1976. Macromolecular mimicry: substances released by sea anemones and their role in the protection of anemone fishes. Pages 433-441 in G. O. Mackie, ed. Coelenterate ecology and behavior. Plenum Press, New York. Smith, W. L. 1973. Record ofa fish associated with a Caribbean sea anemone. Copeia 1973: 597- 598. Springer, V. G. 1958. Systematics and zoogeography of the clinid fishes of the subtribe Labrisomini. Publ. Inst. Mar. Sci. 5: 417-492. -- and M. F. Gomon. 1975. Variation in the Western Atlantic c1inid fish Malacoctenus trian- gulatus with a revised key to the Atlantic species of Malacoctenus. Smithson. Contr. Zool. (200). 11 pp. Stanton, G. 1977. Habitat partitioning among associated decapods with Lebrunia danae at Grand Bahama. Pages 169-175 in Proc. Third Inter. Coral Reef Symp., Univ. Miami (R.S.M.A.S.), Miami.

DATEACCEPTED: October 7, 1985.

ADDRESS: (R.T.H.) The Marine Biomedical Institute, 200 University Boulevard, The University of Texas Medical Branch, Galveston, Texas 77550-2772.

BULLETINOFMARINESCIENCE,39(1): 134-138, 1986

EFFECTS OF LOWERED WATER TEMPERATURE ON THE SURVIVAL AND BEHAVIOR OF JUVENILE FRENCH GRUNT, HAEMULON FLA VOLINEATUM

Donald E. Hoss, David S. Peters and William F. Hettler

Temperature reduction associated with natural events or developing technol- ogies may cause substantial impacts in subtropical waters. Natural cold water intrusions have recently been postulated as the cause of mass fish kills. 1 Artificial mixing of cold water (< 10°C)with tropical surface layers is likely if Ocean Thermal Energy Conversion (OTEC) is developed as an alternative source of electrical energy. Impacts of such cold water intrusion are difficult to evaluate because no data are available. Cold shock data are limited to effects measured on juveniles and adults in temperate climates. The specific objectives of this study were to evaluate a simple technique for

'Gulf and Caribbean Fisheries Institute. 1981. Unusual mass fish mortalities in the Caribbean and Gulf of Mexico, an ad hoc symposium, Mayaquez, Puerto Rico, 1981. Prepared by the Atlantic Oceanographic and Meteorological Laboratories, Miami, Florida. 46 pp.