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Sex Change in the Damselfish <I>Dascyllus Reticulatus</I> (Richardson) (Perciformes: Pomacentridae)

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Sex Change in the Damselfish <I>Dascyllus Reticulatus</I> (Richardson) (Perciformes: Pomacentridae) BULLETIN OF MARINE SCIENCE, 46(3): 79()-798, 1990 SEX CHANGE IN THE DAMSELFISH DASCYLLUS RETICULATUS (RICHARDSON) (PERCIFORMES: POMACENTRIDAE) Abby L. Schwarz and C Lavett Smith ABSTRACT Dascyllus reticulatus, the two-stripe or reticulated damselfish, is shown to be a protogynous hermaphrodite on the basis of the histology of its gonads. Small females have no apparent presumptive testicular tissues but older females show various degrees of proliferation of spermatogenic crypts (=cysts), and oocyte remnants are visible in all but the largest males. Males retain the ovarian lumen and a separate sperm duct develops in the gonad wall. There is no evidence for prematurational sex change in this species. Small transitional fish were present within each group examined, and in all but one case they were smaller than the largest females in their groups. Their presence may be the consequence of a strategy by which such individuals gain some reproductive advantage. We suggest as one possibility that they become the dominant males in groups of smaller conspecifics, including groups newly-settled from the plankton which presumably lack males. Sequentially hermaphroditic species are known from a number offish families, but until recently only the family Sparidae was known to include both protandrous and protogynous species. It is now clear that the Pomacentridae also exhibits both types of sequential hermaphroditism. Protandry was reported by Moyer and Naka- zono (1978), and Fricke and Holzberg (1974), Schwarz (1980), and Coates (1982) have provided indications of protogyny. Shpigel and Fishelson (1986) presented somewhat equivocal histological evidence for protogynous sex change in Dascyllus aruanus and D. marginatus but reported that when the male of a group was removed, the largest female transformed into a male. Dascyllus reticulatus, the two-stripe or reticulated damselfish, is a small plank- tivorous diurnal pomacentrid that ranges from East Africa to Pitcairn Island and from New Caledonia to southern Japan. Though widespread in Melanesia and Micronesia, it is absent from the Hawaiian Islands (Randall and Allen, 1977). Single individuals, pairs, or groups to over 50 fish commonly occupy branching corals, usually of the genera Acropora, Pocillopora or Stylophora, which they use for shelter and defend against some conspecific and heterospecific visitors. Ob- servations by ALS at Lizard Island, Australia indicate that the fish are site-bound to a fair degree. Wickler (1976) described spawning behavior in the field. The male cleans a spawning site on coral rubble or on the dead portion of the base of his home colony or (in the absence of coral) on a flat rock surface and displays toward nearby females, who deposit their eggs at that site. One female may spawn with several males, and a male's nest may contain the eggs of several females. After spawning, the male drives the females away and guards the demersal adhesive eggs until they hatch 2-2.5 d later (25°C). During embryogenesis the male pe- riodically fans the eggs with his pectoral fins; if he is prevented from doing so, fungus quickly destroys the clutch. The larvae are planktonic, so it is unlikely that they are recruited to the same areas where they were hatched, and the recruits at a given locality are not apt to be siblings or even to have been spawned in the immediate vicinity. Dascyllus reticulatus is sexually monomorphic. The only reliable methods by which the sexes can be distinguished are histological examination of the gonads 790 SCHWARZ AND SMITH: DAMSELFISH SEX CHANGE 791 and observation of spawning. The signal-jump or dip, usually only performed by males during courtship or aggressive displays, is sometimes executed by females or transitional fish during aggressive interactions (Schwarz, in prep.). Behavioral evidence for protogyny in this species, including observations on marked individuals that spawned as females and then, after removal of the largest male in each group, as males will be presented in a forthcoming paper (Schwarz, in prep.). In this paper we provide histological evidence for protogynous sex change in D. reticulatus. We also report the presence of small individuals with trans- forming gonads within social groups and suggest that at least some of these in- dividuals may become the dominant males in groups of smaller conspecifics, including groups of newly-settled juveniles. MATERIALS AND METHODS Observations on and collections of D. reticulatus were made by the senior author at One Tree Island, Australia in January 1984 and at Guam in September 1985. All individuals inhabited branch- ing corals (Acropora isopora and Pocillopora damicornis in Australia; Pocil!opora eydouxi in Guam) surrounded by sand (Australia) or rock pavement (Guam). Fish were captured by anesthetizing them with a I: 10 solution of quinaldine in acetone. Standard length (SL) was measured to the nearest mm. The gonads and associated structures were excised and preserved in Bouin's fixative or 10% buffered formalin for 24 h before transfer to 70% isopropanol or ethanol. The gonads were embedded in Parowax, sectioned serially at 5-7 !lm, and stained with hematoxylin and eosin. The specimens from Guam (G-I through G-16) represented three groups captured intact at 7.6 m depth. These groups were the only D. reticulatus found in 2 weeks of diving, and they were not observed prior to collection. The Australian specimens (A-I through A-23) comprised three groups captured intact at 6 m depth and maintained in separate mesh cages 10m apart at that depth for 46 days (as part of;!n experiment to be reported later; Schwarz, in prep.). After 4 days of observation the largest fish was removed from each group, sacrificed, and its gonads examined under a dissecting microscope. The remaining fish were kept under observation until they were collected and sacrificed 6 weeks later. RESULTS Data for the three Australian groups exclude the largest fish in each group as these fish were removed 4 days after caging. Each of these three individuals proved upon gross examination to be a mature male with large testes full of sperm. When the remaining caged fish were examined 6 weeks later, the largest fish in two of the three groups was a mature male. Since the spawning history of these groups was unknown this cannot be construed as evidence for sex change. As the Guam groups were the only groups of D. reticulatus found, we do not know at what point they were collected relative to the breeding season of other Guamanian D. reticulatus. However, our data (Tables 1, 2) indicate that the fish in these groups were well past their breeding season. During the field work at One Tree Island, uncaptured groups of fish were observed spawning, indicating that the Australian groups were collected during their breeding season. The experi- mental groups included ripening as well as post-spawning and resting individuals (Tables 1, 2). The general form of the gonad of both sexes was that of a perciform ovary (Smith, 1965; Hastings, 1981). The reproductive tract was Y-shaped with a short common oviduct forming the stem of the Y. The gonads were completely encap- sulated with a muscular wall. Germinal tissue surrounded the lumen anteriorly, but posteriad the ventral part of the wall was free of gametogenic tissue, as was the common oviduct. The germinal tissue was arranged in low, rather irregular, longitudinal lamellae. As the gametes developed, the lamellae became distended until the lumen was nearly occluded in spawning fish. 792 BULLETIN OF MARINE SCIENCE, VOL. 46, NO.3, 1990 Table I, Histologic profile of gonads of males and transformed fish SL Oocytes ID No. (mm) (III, IV, V)** Spermatocytes Sperm Interpretation Males G-6 60 4,4,4 2 I inactivet A-I 60 I 3 ripe A-23 60 I 3 ripe A-17 58 I 3 ripe Transforming G-3 51 1,-,- 2 2 inactive, ~* G-IS 49 4,4,4 I 2 recently spawned as ~ G-l2 38 4,4,4 2 2 recently spawned as ~ Ie __ A-3 52 , , 3 1 inactive, ~ A-4 47 4,4,4 1 2 recently spawned as ~ A-19 44 4,4c,_ 3 I recently spawned as ~ A-IS 41 1,-,- I I inactive, ~ I: Rare. 2: Comnlon-numerous and visible in all sections. 3: Abundant-aU spenn passages filled and gonad noticeably distended. 4: Degenerating. c: Chorionic adhesive threads visible. *: Refers to last functioning sex. .•••: See text for explanation of staging. t: No active vitellogenesis or spermatogenesis apparent. Females. - Twenty-six specimens were examined (Tables 2, 3; Fig. lA). The 00- cytes first became recognizable as enlarged cells surrounded by follicle cells. As the oocytes continued to grow, their cytoplasm became strongly chromophilic and multiple nucleoli appeared around the periphery of the nucleus. We arbitrarily designated these as stage I oocytes if the darkly-staining cytoplasm layer was thinner than the diameter ofthe nucleus. Larger cells in which the cytoplasm layer was thicker but still darkly stained were designated as stage II. Stage III cells had cytoplasm which was distinctly paler than that in stage II. In early stage III oocytes, the cytoplasm was solid; later, vacuoles developed, probably as the result of the formation oflipid yolk. In the later stages the chorion also thickened and became radially striated and a reticulum of thick strands formed between the chorion and the follicle cells. This structure apparently ac- counted for the adhesiveness of the newly-laid eggs. Stage IV oocytes were much larger, with yolk that consisted of spherules (the protein yolk). In stage V oocytes, the protein yolk spherules disappeared and the cytoplasm became uniformly finely granular. Fully developed stage V oocytes were not seen in the follicles in our material, but were present as ovulated eggs free in the lumen.
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