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Reproductive Biology of Pigmy Angelfishes of the Genus <I

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Reproductive Biology of Pigmy Angelfishes of the Genus <I BULLETIN OF MARINE SCIENCE. 31(3): 495-513. 1981 REPRODUCTIVE BIOLOGY OF PIGMY ANGELFISHES OF THE GENUS CENTROPYGE (POMACANTHIDAE) J. A. Bauer Jr. and S. E. Bauer ABSTRACT Centropyge are long lived territorial coral reef inhabitants which adapt well to aquaria for extended periods (8+ years). They are well suited for reef and laboratory study of reproductive behavior and may also serve as a model for pomacanthids in general. The spawning behavior of six species of Centropyge. including two Atlantic and four Pacific species, was studied in the laboratory for periods of 4 to 7 years. Extensive coral reef observations were made of three species of Centropyge. Harem groups of the same fishes were observed on consec- utive days on their reef territory. The proposed "Continuous Spawning Strategy" is distinct and different from marine spawning strategies described previously and consists of a well-sustained, stress-free, daily gamete production and results in larval dispersal which is maximal and continuous. Based on reef and tank observations, Celltropyge spawning consists of: (I) a crepuscular spawning ritual, which is (2) a regular d:!qy activity of the harem group and (3) usually results in spawn- ing, but may have other functions as well. (4) Each female spawns a moderate number of eggs every day continuously throughout the year or during a season depending on latitude. (5) Territory has predominantly reproductive significance and is defined by the spawning ritual. (6) Each female spawns only once each day with the harem male. (7) The spawning ritual provides defense from predation. Embryogenesis of Celltropyge is presented. Egg size (0.6 mm) and development of all species studied in tank or on reef are similar; pigment distribution may aid in species identification early in development. Hatching occurs in 30-32 h at 20_24°C resulting in very primitive larvae; yolk is absorbed by 100 h when the larvae are 2 mm. Sustained fecundity defined as eggs/fish/day, is in the range of 56-119, and expresses the continuous rate of gamete production. The reproductive strategy of pomacanthid angelfishes has not been defined. Commercial interest in pomacanthids is based on their value as highly desirable ornamental aquarium fish. It is therefore not surprising that the first recognition of spawning behavior in any pomacanthid was made in an aquarium setting (Bauer and Klaij, 1974). It also follows that this initial observation was made on pigmy angels, Centropyge bispinosus, rather than in the much larger wide-ranging an- gelfishes. Knowledge of reproduction in the larger angelfishes is scant; Munro et al. (1973) studied ovarian histology to assess their spawning season; Moe (1976, 1977) described the embryogenesis and succeeded in rearing some of the larger pomacanthids. Bauer and Klaij (1974) described four previously unreported observations: (1) the spawning behavior of a pomacanthid, (2) the characteristic spawning posture of Centropyge bispinosus, (3) a description and photomicrograph of Centropyge eggs, and (4) the possibility of daily spawning in coral reef fish. Subsequently, we studied additional Centropyge species in tank and on reef (Bauer and Bauer, 1976) and found their behavior identical to C. bispinosus. A uniform pattern emerged suggesting a reproductive strategy distinct and different from the usual conception of pelagic spawning in marine fishes. Stimulated by these observations, Lobel (1975) confirmed our findings through reef observations of an endemic Hawaiian species of Centropyge and also intro- duced the possibility of lunar spawning periodicity (1978). Moyer and Nakazono 495 496 BULLETIN OF MARINE SCIENCE, VOL. 3\, NO.3, 198\ Table I. Celltropyge spawning groups observed in aquaria Spawning No. Groups Fish Harems Years'" Pairs Years· Atlantic Species C. argi 4 10 MMFFt 2 MF 2, 3, 5 C. acanthops 2 6 MFFF I MF 2 Pacific Species C. bispinosu.~ I 3 MFF 1Y.z C. j/al'issimus 2 4 MF 2,7 C. /oriculus 3 6 MF I, IY.z,3 C. fisheri 2 5 MFF MF 2Y.z Totals 14 34 4 10 .•.Approximate years spawning groups were maintained and periodically studied intensely. t After seveml months. increasing harassment necessitated removal of the smaller male. (1978) also observed a similar reproductive behavior and made the interesting discovery of protogynous hemaphroditism in C. interruptus. The present investigation compares the population structure, courtship, spawn- ing behavior, fecundity, and egg and larval development in seven species of Atlantic and Pacific Centropyge angelfishes. Our findings are based on extended aquarium as well as reef observations and form the basis for our suggested con- ception of the reproductive strategy of Centropyge. MATERIALS AND METHODS Laboratory Experiments Spawning groups of six species of Centropyge were maintained in 180-1aquaria in synthetic sea water (Instant Ocean), at a salinity of 27-3()o,{,o. Water quality was maintained by water changes of 10% per month and by brisk airlift filtration over a crushed oyster shell substrate, at ambient room temperature (20-24°C). Extended spectrum fluorescent (Grolux) illumination at I watli5 I was main- tained on a timer for 14-16 h/day; additionally, all tanks had exposure to natural daylight cycles. Mats of filamentous green algae coating substrate and walls, as well as dense growths of CauJerpaj/oridana, provided ample grazing areas and probably improved water quality. Several feedings per day of dry flake food (Tetramin) were supplemented with shredded scallop and shrimp, adult frozen Artemia salina, and frozen fish eggs. Celltropyge studied included two Atlantic species, C. argi and C. acanthops, and four Pacific species, C. bispinosus, C.fisheri, C.j/al'issimus, and C. loricu/us; fourteen separate spawning groups consisting of 34 fish were observed in captivity for periods of I to 7 years (Table I). Spawning behavior was documented by visual observations, cine and still photography, and by egg colIections. Eggs were collected by recirculating the aquarium water through a 295 ILmnet beginning Y.zh before spawning and continued for 6-8 h. Collected eggs were counted and fertility determined. The aquarium study was conducted along four observational plans: (I) daily observation of spawn- ing behavior; (2) egg colIection at random periods throughout the year to confirm actual gamete discharge folIowing observed spawning behavior; (3) consecutive nightly egg sampling to confirm sustained spawning continuity; and (4) quantitative egg collections on consecutive days to determine numbers of egg produced per female each day. Field Experiments Reef observations of the Atlantic C. argi and Pacific C.j/al'issimus and C. bic%r were conducted during various periods throughout the year in Curacao, Grand Cayman, Enewetak, Tahiti, Bora Bora and Lizard Island. Observations of colonies of Centropyge were made at 3-18 m throughout alI periods of the day and night including 120 h during the sunset crepuscular period. Observation sites were selected to permit continuous closeup (1-2 m) overview of the entire ter- ritory of a spawning group; sites were marked to facilitate consecutive daily observation of the same individuals. Three groups of C. argi were studied repeatedly from 6 to 16 days; three harem groups BAUER AND BAUER: PIGMY ANGELFISH REPRODUCTIVE BIOLOGY 497 Table 2. Reef spawning observations Observation Spawning Consecutive Spawning Species Site-Year Group Days Month Moon C. argi Curacao 77 MFFF 16* 5,6 )O( Curacao 78 MFFF 14* II, 12 0(. Curacao 79 MFFF 7* 12 ) Cayman 80 MFF 6 I • C. j/avissil1llls Enewetak 75 MFFF 12 5, 6 )O( Tahiti 78 MFF 10* 8,9 O( C. hic%r Australia 80 MF 5 8 (. • Two different spawning groups observed by separate observers at the same time. O-full moon, )-151 quarter, .-new moon, (-last quarter. of C. j/avissil1llls were observed from IO to 12 consecutive days; and one pair of C. hie%r was observed for five consecutive days (Table 2). Observed reef spawning was documented by cine and still photography and confirmed by egg collections; a 375 ILm plankton net (mouth diameter of 0.75 m) was swept through the water over the spawning site immediately after observed spawning. Since collection efforts could disrupt natural spawning behavior, egg collection was done only from the last female to spawn in the harem group each night and only during the last few days of each observation period. Egg counts and fertility ratios were determined on 17 reef collections. Developing eggs and larvae were maintained in one liter jars of artificial or natural sea water with minimal or no aeration. Eggs were measured using an ocular micrometer and from photographs taken at 50x and 100x magnification using an ED- IO Polaroid Instrument Camera. RESULTS Spawning Frequency Aquarium observations show a pattern of continuous daily spawning in all six Centropyge species studied for periods of several years. Four observational ap- proaches yielded consistent findings: (1) nearly continuous observations of 14 spawning groups for up to seven years showed daily spawning behavior, (2) random periodic egg collections documented the actual presence of fertile eggs whenever randomized sampling was performed (Fig. 1); (3) consecutive daily egg collections for periods up to 120 days also confirmed daily spawning; (4) the daily spawning of every female in a harem grouping was confirmed by quantitative egg collections which show the daily recovery of twice as many eggs from a tank containing two females and a male, than from a similar tank holding only a pair (Fig. 2). Each female was observed to spawn only once each evening. Spawning continuity, however, depended on the maintenance of adequate nu- trition and aquarium water conditions; our observations suggest that when these factors were allowed to deteriorate for short periods, courtship activity was main- tained but appeared not to result in spawning on each day. Reef observations also indicate continuous daily spawning of three species of Centropyge.
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