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<I>Anthias Squamipinnis</I> BULLETIN OF MARINE SCIENCE, 31(2): 383-398, 1981 CORAL REEF PAPER SEQUENCE OF COLORATION CHANGES DURING SEX REVERSAL IN THE TROPICAL MARINE FISH ANTHIAS SQUAMIPINNIS (PETERS) Douglas Y. Shapiro ABSTRACT The color pattern of females of the protogynous fish Anlhias squamipinnis contrasted strongly with the color pattern of males. Both in the laboratory and in the field, females were induced to change sex by removing a male from their social groups. Color changes of the sex-reversing fish occurred in two phases: a short term phase, in which the basic pattern of male coloration was laid down in black or black-violet pigment; and a long term phase during which the black-violet coloration became progressively paler and more purely red or red- violet. During the short term phase in the laboratory, color changes appeared first on the pelvic fins or in the head-nape region, next on the dorsal fin or in the superior pectoral region, then on the caudal fin, and finally in the inferior pectoral region. The day-by-day sequence of changes was characterized by an early onset (3-6 days after male removal), a short interim period (2-11 days), and a short total time for completion (7-16 days after male removal). 75% of 44 sex reversals in the lab and in the field followed this typical sequence. Sequences in the field were slightly more prolonged than sequences in the laboratory. Two atypical sequences characterized the remaining sex reversals. Differences in the temporal characteristics of color change sequences appeared to be related primarily to differences in the social circumstances surrounding the initiation of sex reversal. It appeared likely, there- fore, that social factors could influence the sequence of coloration changes during sex re- versal. Among protogynous marine fishes, i.e., species in which individual females change into males during their adult life, many are sexually dichromatic (Atz, 1964; Reinboth, 1970; Smith, 1975; Robertson and Warner, 1978; Warner and Robertson, 1978). In these species, sex reversal involves an alteration of a fe- male's coloration, gonadal function, and behavior (Shapiro, 1979). Coloration may change approximately in synchrony with gonadal restructuring, as in certain Scaridae, Labridae. and Anthiinae (Choat, 1969; Popper and Fishelson, 1973; Robertson and Warner, 1978; Shapiro and Lubbock, in preparation), or may at least partiaIly precede (Gundermann, 1972; Roede, 1972; 1975) or succeed it (RandaIl and RandaIl, 1963; Quignard, 1966; Buckman and Ogden, 1973). Mor- phological changes in fish coloration, including those accompanying protogynous sex reversal, are generally thought to be hormonaIly controIled (Okada, 1962; Reinboth, 1962b; reviews by Odiorne, 1957; Fujii, 1969). While the color changes foIlowing androgen treatment of females have been briefly described for several protogynous species (Stoll, 1955; Roede, 1972; Fishelson, 1975), the fuIl sequence of color changes in individual fish undergoing natural sex reversal has not received careful scrutiny. In the protogynous, Indo-Pacific serranid, Anthiinae fishes, external differences between males and females are seen generally in body size, fin length, and most strikingly, in coloration (Lubbock and Allen, 1978; RandaIl, 1979; Randall and Lubbock, in press). Anthias squamipinnis is a smaIl, shaIlow water, coral reef species which lives in stable social groups with a median sex ratio of eight adult females per male (Shapiro, 1977b). Sex reversal in a female can be initiated by the removal of a male from her social group (Fishelson, 1970; Shapiro, 1979). This species has served as the subject for a variety of studies on the ecological, 383 384 BULLETIN OF MARINE SCIENCE. VOL. 31, NO.2. 1981 social, and behavioral aspects of sex reversal (Fishelson, 1970; 1975; Gunder- mann, 1972; Popper and Fishelson, 1973; Shapiro, 1977a; b; 1979), but descrip- tions of its coloration remain limited (Peters, 1855; Klunzinger, 1884; Fowler and Bean, 1930; Smith, 1961; Popper and Fishelson, 1973). The aims of this paper are: (I) to describe in detail the coloration of male and female A. squamipinnis; (2) to describe the sequence of color changes accom- panying gonadal and behavioral sex reversal initiated by the removal of a male from a social group; and (3) to comment on changes in size and fin length. The sequence of color changes will be examined both in naturally occurring and in artificially established social groups. MATERIALS AND METHODS Laboratory Study The description of male and female coloration was based on approximately 20 males and 120females kept in laboratory tanks over a 3-year period and was modified to include variations from that pattern observed during five months of field study in the Red Sea and Indian Ocean. For a description of the color changes of sex reversal, four social groups, each containing one male and six adult females, were established in separate aquaria. After a 2-month baseline period the male was netted and removed from two of these groups while, in the other two groups, the male was netted and released. Thirty-five days later the male was removed from the groups first used as controls and a control manipulation performed in the originally experimental groups. This procedure was repeated until a total of eight males had been removed from the four groups and, in response, seven females had changed sex (Shapiro, 1977a; 1981). The aquarium size, illumination, water temperature, pH, and specific gravity, feeding routine, general maintenance, detailed methods of experimental proce- dure, and the gonadal histology and behavioral results of these experiments are described elsewhere (Shapiro, 1977a; 1979; 1981). The sequence of color changes shown by six of the seven sex-reversing fish and, in certain instances, by other females that changed sex in similar laboratory experiments, were described in detail. In each group, individual fish were distinguished and identified by peculiarities of size, hue, fin shape, scars, and eye stripe configuration. Prior to male removal all individuals were visually inspected every few days, through the glass wall of the aquarium, for any change in coloration. The day of male removal was counted as day zero. Subsequently, all individuals were inspected daily until coloration changes were noted on one female. Thereafter, this fish was inspected daily while other group mem- bers were inspected approximately on alternate days. For the sex-reversing fish, the day of appearance of the earliest detectable change in coloration was noted for five body regions which, in the male, show characteristic coloration: head-shoulders (the nape and the anterior part of the dorsal body contour to approximately below the sixth dorsal spine will be called the "shoulders" of the fish), pelvic fins, the posterior sixth of the dorsal fin, the superior and inferior regions of the pectoral fins, and the caudal fin. A record was also made of the day when the basic changes in each region were considered complete. For the caudal, pelvic and dorsal fins the criterion for completion was that the new coloration completely covered that portion of the fin which was typically colored in the male. For the superior pectoral region the criterion for completion was that the dark spot, which developed from discrete, thin, black lines (see Results), was fully confluent. For the head-shoulders region, coloration was considered complete when new, dark pigment covered the region smoothly and con- fluently in a typical male pattern. When all of these areas were judged complete the basic coloration change during sex reversal was considered at an end and the date was recorded. Black and white photographs were taken of males, all females considered likely to change sex (on the basis of size and dominance) and at least one female considered not likely to change sex, prior to each experimental male removal and at least once during or after the subsequent sex reversal. Photographs were also taken of specific individuals at various stages of sex reversal. Finally, when a male was removed from his group, he was anesthetized with MS-222 Sandoz (Bell, 1964) and photographed in color, alive, under magnification and standard illumination, for details of fin and body coloration. At the end of the study, several females were photographed in this way as well. Field Study The color changes of 26 sex-reversing fish in natural groups were examined on Harvey Reef in the Sudanese Red Sea and at two sites on Aldabra Island in the Indian Ocean (for details of the study sites, see Shapiro, 1977a; 1981). Most of these sex reversals followed experimental male removals SHAPIRO: SEX REVERSAL COLOR CHANGES 385 Figure I. A. squamipinnis (from a painting by W. B. Amos). Male (above), female (below). performed as part of other studies (Shapiro, 1979) and could be dated precisely from the day of male removal. All females in each such group were approached daily after male removal, with a few missed days, to within 2 m and scrutinized for color changes. The day of first appearance of color change was called the onset day. Onset day and completion times were recorded for each sex changing fish. Criteria for judging the completion of color changes were the same as those used in the laboratory study. Several sex reversals followed the natural disappearance of males from social groups and a few sex reversals were either already in progress at the start or were still not complete by the end of the study. For the latter, a minimum time could be specified for the duration of color change, but neitherthe onset day nor the completion time could not be specified. Such cases will be noted specifically in the results. 386 BULLETIN OF MARINE SCIENCE. VOL. 3\, NO.2. 198\ RESULTS Female Coloration The entire head and body of females are uniformly orange-gold except the ventral head and body contours which are pale white-yellow (Fig.
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