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Population Structure,Reproductive Behavior and Protogynous Hermaphroditism in the Angelfish

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Population Structure,Reproductive Behavior and Protogynous Hermaphroditism in the Angelfish Japanese Journal of Ichthyology 魚 類 学 雑 誌 Vol.25,No.11978 25巻1号1978年 Population Structure,Reproductive Behavior and Protogynous Hermaphroditism in the Angelfish. Centropyge interruptus at Miyake-jima,Japan Jack T.Moyer and Akinobu Nakazono Received January 14,1978)( Abstract.Population structure,reproductive behavior and protogynous sex inversion of the angelfish Centropyge interruptus was studied in the waters of Miyake-jima,Japan.A single male dominates a harem of from one to four females,with the size of the harem being dependent upon the nature of the substrate.Females are controlled by aggressive herding by the single male.Six action patterns associated with maintenance of dominance by the male and with courtship are described.These include(1)rushing,(2)circling,(3) soaring,(4)mutual soaring,(5)nuzzling,and(6)spawning.Spawning usually takes place almost every day at approximately sunset during the period from May to October. Removal of the male resulted in sex change by the ranking female.Histological ex- amination of the gonads confirmed field observations of protogynous sex inversion.The histology of the gonads of females,males and intermediate individuals is described. Studies of reproductive strategies and popu- representatives of the various angelfish genera lation structures of pomacanthid fishes are may eventually provide useful tools for clas- scarce.Lobel(1975),Shen and Liu(1976)and sification of this difficult family. Suzuki et al.(1977)have reported on various The population structure and reproductive aspects of reproduction in the genera Centro- behavior of Centropyge interruptus were studied pyge and Genicanthus.Most of these studies near the Tatsuo Tanaka Memorial Biological have been based mainly on aquarium observa- Station(TMBS)at Miyake-jima(34•‹05'N, tions and do not cover all aspects of repro- 139'30'E),one of the Izu Islands,from early ductive behavior.Population structure re- July,1976,to the end of the spawning season mains unknown for any of the Pomacanthidae in October,1977.Histological studies of (Ehrlich,1975). gonads were made at the Fishery Research Since the taxonomic revision of the angel- Laboratory of Kyushu University.This paper fishes by Fraser-Brunner(1933),considerable reports the results of these investigations. controversy has appeared in the literature concerning the classification of angelfishes. Methods and materials Yasuda and Tominaga(1970)united Genicanthus The social behavior of Centropyge interruptus with Holacanthus;however,Randall(1975) was investigated daily from July to September, preferred to follow Fraser-Brunner(1933)in 1976-77.Observations were limited to 2-3 separating them into two genera.Centropyge dives per week from September to June in interruptus(Tanaka)was long erroneously both years.More than 300 hours of observa- identified as C.fisheri Snyder.Holacanthus tions in nature were made using SCUBA. interruptus was resurrected by Tominaga and Social interactions were recorded while lying Yasuda(1973);however,Randall and Wass on the bottom within the territory of the (1974)placed the species in Centropyge, social group under study.Individual fish partly on the basis of feeding habits.We were not marked,but could be identified by have followed Randall and Wass(1974)as a location,individual variations in color pat- result of observations reported in this paper. terns,and individual behavior.Water tem- Detailed studies of both the reproductive peratures were read from commercial diving units and courtship behavioral patterns of guages.Forty specimens ranging from 86 to •\ 25•\— 魚類学雑誌 Japan.J.Ichthyol.25(1),1978 150 mm in standard length were taken with and embedded in paraffin.They were cut screen nets and multi-pronged spears.They at 7p in cross section and stained with were fixed in 10%formalin and measured. haematoxylin and eosin.Their structure and The gonads of all specimens were removed sex were examined under a microscope.All Fig.1.Map of the study site at Igaya Bay, Miyake-jima,showing relative locations, dimensions,and depths of Centropyge interruptus territories of the males of Harems A•`O.Note changes in A and B between July and August,1976,and between 1976 and 1977(explanation in text).Harems C•`O remained the same in both years. •\ 26•\ Moyer and Nakazono:Behavior of Centropyge interruptus fish specimens are deposited at the Tanaka Table 1.Population structure of Centro- Memorial Biological Station(TMBS)and pyge interruptus at Igaya study site, gonad specimens are at the Fishery Research Miyake-jima,Japan,1976 and 1977. Laboratory,Kyushu University. Results Centropyge interruptus is a protogynous hermaphrodite that lives in a harem social structure with one dominant male and from 1 to 4 females per reproductive unit.The size of the harem and the intensity of territorial defense is directly influenced by the habitat. Habitat and population structure.Centro- pyge interruptus occurs in a variety of habitats at Miyake-jima.All habitats are dominated by boulders and/or lava cliffs.Although there are often outcroppings of corals within a particular anglelfish's territory,C.interruptus, unlike other members of the genus,is not a coral reel fish.In fact,in areas of extensive Acropora corals,the species is scarce or lack- ing altogether. Three distinct habitat types were noted,i.e. (a)tunnels and arches,(b)volcanic cliffs,and (c)large boulders.The density of populations of Centropyge interruptus appears to be directly influenced by the nature of the habitat. Crevices,cracks,and holes along the ceiling and walls of tunnels and arches provide maxi- mum shelter,and population densities are greatest at such locations.The main center increased from 9 to 18 m,with shallow points of activity of one male and his harem of at the cliff-top varying considerably between four females at the Abe Tunnel was restricted 5 and 12 m(Fig.1).Including in this area to an area of about 5m•~3m,directly below were a maximum of 15 harems in 1976 and the ceiling of the tunnel,which consisted of 14 harems in 1977.The population structure a complicated network of crevices and cracks. within each harem is shown in Table 1,with This tunnel,a dark cavern 21m•~5m•~14m territorial sizes and respective locations ap- and ranging in depth from 16 to 20 m,con- pearing in Fig.1. tained five harems totaling 22 fish(5 males, Sexual dichromatism.Previously unde- 17 females).Volcanic cliffs are also heavily scribed sexual dichromatism in this species eroded into crevices,holes,and caverns,and, makes sexual discrimination obvious at dis- like arches and tunnels,support dense popula- tances up to 10 m or more,even by the tions of C.interruptus.Boulder habitats human observer(Figs.2,5).The opercular provide less cover and display the lowest region of females is primarily orange,flecked population densities,with the reproductive with small blue dots.The posterior soft unit usually a monogamous,but unstable dorsal and anal fins are dark blue.Males pair. have heavy blue lines in the opercular area, Our chief study site was situated along an making the head appear blue from a distance eroded volcanic cliff;running seaward for of several meters.The posterior soft dorsal 190 m outside the fishing port of Igaya(Fig.1). and anal fins are streaked with broad,irregular Depths at the foot of the cliff gradually bright blue bands on a black background, •\ 27•\ 魚類学雑誌 Japan.J.Ichthyol.25(1),1978 easily visible from 10 m or more. Fish species with colors resembling C. Territoriality.Males vigorously defend interruptus were often momentarily rushed. their territorial boundaries against neighboring Such encounters apparently resulted from males.Boundaries are easily defined by a mistaken identity,suggested by the fact that particular boulder,crevice,or lava pinnacle, the rushing male would suddenly stop several and are seldom violated.However,occasional- meters from the object of his attack and ly during courtship,a male will enter another return to feeding.Presumably,the rushing male's territory to rush(Fig.4A)a female male mistook the other blue species as a from the neighboring harem.Such intrusions member of his harem.Rather than territorial are met by aggressive chasing by the defend- defense,rushing of this nature is related to ing male.Visiting females from neighboring the establishment and maintenance of domi- harems are rushed and circled(Fig.4B)but nance,and will be discussed below.Species are rarely driven from the territory. rushed in this manner included the damselfish Sex-distinguishing colors play an impotant Pomacentrus coelestis Jordan et Starks,adults of role in courtship behavior;but,in addition, the wrasse Coris gaimardi(Quoy et Gaimard), they appear to elicit aggression between neigh- and the angelfish Centropyge bispinosus boring males.Encounters between rival (Gunther). males at territoral borders often result in With the exception of C.bispinosus,which broadside posturing,head to tail,fins ex- appears a velvet blue at depths of 10 m or tended to clearly show sex-distinguishing color more,other congeners were tolerated.Various patterns. male C.interruptus in the study site shared Females respond somewhat agonistically their territories with C.tibicen(Cuvier),C. toward outside females,but no more so than ferrugatus Randall et Burgess,and C.vrolicki toward other female members of their own (Bleeker). harem.Encounters with females from neigh- Establishment of dominance and sex inver- boring territories are relatively rare,and sion.Observations in the field revealed the occur only when feeding brings them into relationship between sex inversion and the close proximity to each other.Then the social system of this species.On Oct.10, home female rushes and circles the visitor, 1976,aquarium hobbyists collected the male invariably causing the outsider to flee to the and one of four females from Harem A and safety of familiar shelter holes.This cannot both females from Harem B(Fig.1,Table 1).
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