Status-dependent behavioural sex change in a polygynous coral-reef fish, Halichoeres melanurus

To examine how a change in an individual's social status could influence its behavioural sex, we conducted male "removal-and-return" experiments in the polygynous wrasse, Halichoeres melanurus. This coral-reef fish is a protogynous hermaphrodite: the largest female (LF) living in a male's territory typically completes functional sex change within 2–3 weeks after the male's disappearance. In this experiment we removed males from their territories just prior to spawning time, about 1 h before sunset. In 12 of 30 trials, the resident LF spawned in the male role with smaller females, 21–98 min after male removal. Previous research suggests the LF should readily adopt male sexual behaviour to retain smaller females as future mates. However, the LFs of smaller body size were less likely to immediately perform male-role behaviour. This could be related to females' preference for larger mates: smaller LFs would be less likely to be chosen by other females, even if they could complete sex change and defend a territory. When a male was returned immediately after an occurrence of female–female spawning, the LF subsequently spawned in the female role with the returned male (6 of 12 trials). It could be adaptive for the LFs to accept a larger male as a mate rather than to fight against it. Thus, behavioural sex is reversible in H. melanurus, changing rapidly with social status. Electronic Publication     

Sexually dichromatic protogynous angelfish Centropyge ferrugata (Pomacanthidae) males can change back to females

Protogynous hermaphroditism, female-to-male sex change, is well known among reef fishes where large males monopolize harems of females. When the dominant male disappears from a harem, the largest female may change sex within a few weeks. Recently, from experiments with some protogynous haremic fishes in which two males' cohabitated, it was confirmed that sexual behavior and gonads were completely reversible according to individual social status. However, the ability to reverse secondary-developed sexual body coloration has never been examined in any protogynous fish. We conducted two male cohabitation experiments with the protogynous haremic angelfish, Centropyge ferrugata, which has conspicuous sexual dichromatism on the dorsal fin. Smaller males of C. ferrugata soon performed female-specific mating behaviors when they became subordinated after losing a contest. They then completed gonadal sex change to females 47 or 89 d (n=2) after beginning cohabitation. In the course of the reversed gonadal sex change, male-specific coloration on the dorsal fin changed to that of a female. Thus, the sex of C. ferrugata, including secondary developed sexually dichromatic characteristics, can be completely reversible in accord with their social status.     

Habitat Patch Size,Facultative Monogamy and Sex Change in a Coral-dwelling Fish, <Emphasis Type="Italic">Caracanthus unipinna</Emphasis>

Synopsis We investigated the inter-relationships between coral colony size, social group size, mating system, and patterns of sex allocation in the pygmy coral croucher, Caracanthus unipinna (Caracanthidae), an obligate coral-dwelling fish. Histological examination of the gonads from all individuals in social groups revealed that the predominant mating system was harem polygyny. However, both group size and mating system co-varied with coral colony size, with pair forming and monogamy occurring on small corals and group forming and harem polygyny on large corals. This species therefore displays mating system plasticity in response to varying habitat patch size. Within-group sexual size dimorphism and individual gonad structure indicate that C. unipinna is also likely to be a protogynous hermaphrodite. These social and reproductive features of C. unipinna contrast with some other coral-dwelling fishes, which display a lack of social and mating system plasticity in response to habitat patch size, and either bi-directional or protandrous sex change. Possible reasons for this dichotomy include differences in spawning mode, parental care and levels of intrasexual aggression.     

A fluvial population of Cottus pollux (middle-egg type) from the Honmyo River, Kyushu Island, Japan

 Specimens of the Cottus pollux species' group collected from the upper part of the Honmyo River, Nagasaki Prefecture, Japan, were subjected to morphological and allozyme analyses to place them into one of the recognized valid taxa, viz. small-egg type (SE type), middle-egg type (ME type), or large-egg type (LE type). They were identified as ME type on the basis of specific morphological characteristics, such as laterally depressed cross-sectional shape at posterior half of the body and deep caudal peduncle, and by having a diagnostic allozyme allele (MEP ^* 54). This ME-type population is the first recorded from Kyushu Island, Japan. An ecological survey of the population revealed that females spawned larger eggs (2.8–3.2 mm in diameter) than those of other amphidromous populations, from which well-developed yolk-sac larvae of about 8.0 mm TL were hatched out. In addition, ME-type specimens collected on 25 and 26 May 2001 included 15 sex-unknown juveniles ranging from 18.8 to 30.2 mm SL, suggesting that they represented larvae hatched out on a nearby spawning ground, with no experience of downstream migration into Isahaya Bay. This observation strongly suggests that the ME-type population in the Honmyo River has a fluvial lifestyle, being different from other amphidromous populations. The former population may have arisen from an amphidromous ancestor through changes in egg size and early ontogenetic development. Received: February 25, 2002 / Revised: May 21, 2002 / Accepted: June 17, 2002 Acknowledgments We thank Professor M. Azuma, Nagasaki University, for his kind guidance of our field survey in the Honmyo River and Dr. G.S. Hardy, Thames, New Zealand, for correcting the English. Thanks are also offered to Mrs. Y. Miyajima and Y. Masaoka, Kyushu Branch of Construction and Technology Institute Co., for their helpful cooperation in the field survey. Drs. H. Sakai, National Fisheries University and Y. Yamazaki, Toyama University, and Mrs. N. Okabe and Y. Suzuki of Yamagata Prefecture are thanked for their help in sample collection. This work was partly supported by a Grant-in-Aid (No. 13660171) from the Japan Ministry of Education, Culture, Sports, Science and Technology to A. Goto. Correspondence to:Akira Goto     

A marking technique for live fish eggs and larvae

 A new marking technique for live fish eggs and larvae was proposed to elucidate the larval biology and adult breeding ecology of wild fish. In the laboratory, females of a freshwater goby Rhinogobius sp. OR were abdominally injected with one of three coloring agents—brilliant blue FCF, rose Bengal, or β-carotene—before their oviposition. The rose Bengal proved lethal to adult fish. The other two dyes had little effect on adult mortality. With these two treatments, there were negative effects on neither fecundity nor egg mortality, resulting in normally developed larvae. The brilliant blue FCF stained eggs and larvae greenish blue whereas the staining effect of β-carotene was unclear. The timing of injection was important in effective staining of eggs and reducing the risk of miscarriage. In conclusion, the brilliant blue FCF was the more useful marker. We discuss what this method can show us about the ecology of wild fish and how this method can be applied to field study. Received: March 6, 2002 / Revised: July 11, 2002 / Accepted: August 14, 2002 RID="*" ID="*" Present address: Center for Marine Environmental Studies, Ehime University, 3 Bunkyo-cho, Matsuyama 790-8577, Japan (e-mail: nokuda@sci.ehime-u.ac.jp) Acknowledgments I am grateful to K. Karino, M. Kohda, and A. Moriyama for giving us valuable advice and to M. Inoue and H. Miyatake for their field assistance. This study was financially supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists. Correspondence to:Noboru Okuda     

Reversed Sex Change in The Haremic Protogynous Hawkfish Cirrhitichthys falco in Natural Conditions

Bi‐directional sex change has recently been reported in a range of reef fishes, including haremic species that were earlier thought to be protogynous (female to male). However, the occurrence of this phenomenon and the social conditions driving the reversion of males to females (reversed sex change) have been poorly documented under natural conditions. Reversed sex change is predicted to occur in low‐density populations where facultative monogamy is common. However, few studies have evaluated this over a long period in such populations. We documented the occurrence of bi‐directional sex change during a 3‐yr demographic survey of a population characterised by small harem sizes in haremic hawkfish Cirrhitichthys falco. New males were derived following a change in sex of functional females (secondary males; n = 3) and juveniles always matured first as females (n = 3). Thus, C. falco exhibited a typical protogynous sexual pattern, consistent with a range of haremic fish species. We observed reversed sex change in two males. In both cases, all the females disappeared from their harems and the neighbouring males expanded their territories to encompass the territories of the sex changers. However, bachelor males did not always revert to females. A dominant male experienced bachelor status twice but regained mating opportunities following the immigration of a female into his territory or by taking a female from a neighbouring harem. Thus, we conclude that bachelor males use reversed sex change as a facultative tactic to regain reproductive status in a haremic mating system. In addition, we discuss the influence of harem size upon occurrence of reversed sex change.     

Female spawning strategy in Rhinogobius sp. OR: how do females deposit their eggs in the nest?

 We tried to elucidate how females of a paternal nest brooding goby Rhinogohius sp. OR deposit their eggs in a nest, using a marking technique for live eggs under laboratory conditions in which male somatic condition, nest space, and mating pattern (monogamous or bigamous) were controlled. Whether females rejected mating was independent of either male quality, such as body size and somatic condition, or nest space. In a situation in which two females were allowed to spawn sequentially with a male, however, females rejected mating at a higher rate when they were the first to spawn than when they were the second to spawn; this is because eggs from first females were more vulnerable to cannibalism by parental males and second females. Even when nest space was limited and thus was occupied by eggs from the first females, second females could deposit all their eggs in the nest by using the minute interspace of existing eggs. In the presence of the parental male, such a female seemed less likely to suffer a cost from increased egg mortality due to crowdedness, still holding the advantage of being the second spawner. Finally, we extrapolated the field breeding ecology of this fish from the laboratory data. It was suggested that a single monolayer brood of the same age usually consisted of eggs from multiple females and thus the mating pattern would be more polygynous than previously expected. Received: March 6, 2002 / Revised: July 11, 2002 / Accepted: August 14, 2002 RID="*" ID="*" Present address: Center for Marine Environmental Studies, Ehime University, 3 Bunkyo-cho, Matsuyama 790-8577, Japan (e-mail: nokuda@sci.ehime-u.ac.jp) Acknowledgments I am grateful to S. Sone and D. Takahashi for giving us useful information and to M. Inoue and H. Miyatake for their field assistance. This study was financially supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists. Correspondence to:Noboru Okuda     

Spawning season and migration of the myctophid fish <Emphasis Type="Italic">Diaphus theta </Emphasis>in the western North Pacific

 The spawning season, spawning grounds, and migration of the myctophid fish Diaphus theta were studied in the western North Pacific, based on seasonal sampling and estimation of hatching dates. The peak abundance of larvae was observed in July in the transition waters between the Oyashio and Kuroshio fronts. The spawning season ranged from late March to early September, with a peak from May to July. Larvae and juveniles <40 mm in standard length were distributed in the transition waters, whereas larger individuals were collected in the Oyashio and the Western Subarctic waters. These results indicate that this species undergoes a horizontal spawning migration from the Oyashio and Western Subarctic waters into the transition waters crossing the Oyashio front. Received: July 11, 2002 / Revised: October 2, 2002 / Accepted: October 15, 2002 Acknowledgments We are grateful to the captains, officers, and crew of FRV Hokko-Maru, FRV Tankai-Maru, and RV Hakuho-Maru for their assistance at sea. We thank Dr. H. Saito and Mr. H. Kasai for their cooperation in field sampling, and Dr. C. Sassa for his assistance with larval fish taxonomy. Correspondence to:Masatoshi Moku     

Occurrence of sea eels of <Emphasis Type="Italic">Anguilla japonica</Emphasis> along the Sanriku Coast of Japan

 The age and migratory history of the Japanese eel, Anguilla japonica, collected along the Sanriku Coast of Japan, were examined using otolith microstructure and analysis of strontium (Sr) and calcium (Ca) concentrations. The mean Sr : Ca ratios from the elver mark to the otolith edge indicated that there were eels with several general categories of migratory history, including sea eels that never entered freshwater and others which had entered freshwater for brief periods but returned to the estuary or bay. This first evidence of the occurrence of sea eels in this northern area indicates that Japanese eels of the Sanriku Coast do not necessarily migrate into freshwater rivers. Received: May 15, 2002 / Revised: August 4, 2002 / Accepted: August 15, 2002 Acknowledgments We thank Messrs. S. Yamane and K. Morita, and crews of the Otsuchi Marine Research Center, Ocean Research Institute, The University of Tokyo, for their assistance in collecting the eels. This work was supported in part by Grant-in-Aid No. 13760138 from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Correspondence to:Takaomi Arai     

A novel sexual pattern in serranid fishes: simultaneous hermaphrodites and secondary males in Serranus fasciatus

Synopsis Gulf of California populations of Serranus fasciatus are composed of functional simultaneous hermaphrodites and males. This is the first serranid known to have this sexual pattern which is functionally intermediate between the typical serranid patterns of simultaneous and protogynous hermaphroditism. Males of S. fasciatus are derived from hermaphrodites by resorption of ovarian tissue and proliferation of the extant testicular band. Distinct sexual roles are evident in spawning events. Hermaphrodites gain female function by pair spawning with males (124 and 125 observed spawns) and rarely with other hermaphrodites (1 of 125). Hermaphrodites gain male function by sneak spawning (9 of 125) and rarely by pair spawning with other hermaphrodites. Males exclusively pair spawned with hermaphrodites. Despite its unusual sexual pattern, S. fasciatus appears allied with other Serranus species based on similarities in gonad morphology.     

Sexual development and reproductive seasonality of hogfish (Labridae: Lachnolaimus maximus), an hermaphroditic reef fish

The seasonality, size, age, colour phases and sexual dimorphism of 13 reproductive classes of hogfish Lachnolaimus maximus are described. Analysis of histological sections of gonads ( n = 1662) confirmed earlier conclusions that L. maximus is a monandric, protogynous hermaphrodite. Sex change was initiated at the end of the spawning season and over a broad range of sizes and ages. It occurred after a functional female phase (postmaturation) and proceeded more slowly (months) than previously believed. Eventually all individuals changed sex to a terminal male phase. Females were batch spawners, spawning as often as every day during winter and spring. There was no evidence of precocious sperm crypts in active females, sperm competition or other alternative male sexual strategies. Mating has been reported elsewhere to be haremic. The sexual development of L. maximus appears to be adaptive in terms of Ghiselin's size-advantage model, which links monandric protogyny and polygyny. The slow rate of sex change, however, poses problems when fishing pressure is high because harvest of a single male has the potential to reduce the reproductive output of an entire harem.     

Alternative spawning tactics of female angelfish according to two different contexts of sex change

Social conditions for sex change and reproductive success werestudied in the haremic marine angelfish, Centropyge ferrugatus,in the coral reefs of southern Japan. In this species the largestfemale in a harem changed sex not only after disappearance ofthe dominant male but also occasionally in his presence. Inisolated harems containing two to three females, strict socialcontrol by the dominant male resulted in females changing sexonly after the male disappeared (takeover sex change). In haremsadjacent to each other, however, takeover sex change did notoccur even when one of the males disappeared. Instead, largeharems including more than four females were formed by fusionof two adjacent harems. In such large harems, the dominant malewas unable to socially prevent the largest female from changingsex later to acquire a portion of the harem (harem-fission sexchange). Females in adjacent harems spawned less frequentlyand tended to grow faster than those in isolated harems, probablyto gain an advantage in dominance status over neighbors of similarsize. Thus, females changed spawning frequencies according tothe two different contexts of sex change. The takeover tacticresults in higher fitness than the harem-fission tactic, whichshould be the best in the bad situation of adjacent harems.     

Harem structure of the protogynous angelfish, Centropyge ferrugatus (Pomacanthidae)

Social structure of the protogynous angelfish, Centropyge ferrugatus, was examined on the coral reefs of Sesoko Island, Okinawa, Japan. Each individual male monopolized a harem of 1-6 females. Harems could be categorized as linear-type or branching-type based upon spatial and dominance relationships among the females. A linear harem consisted of different-sized females whose home ranges overlapped each other with a linear dominance order based on body size. Branching harems were composed of two linear sub-groups dividing a male's territory. Females of similar size did not have overlapping home ranges, which resulted in branching harems. These two systems appear to be a result of competition for opportunities of sex change, as only the largest fish of a harem (or a sub-group) can become a male. Comparison of the harem structures of some reef fishes suggests that the two harem structures may occur broadly in protogynous haremic fishes.c/o Prof. T. Kuwamura     

Does gonad structure reflect sexual pattern in all gobiid fishes?

Synopsis In immature and adult females of protogynous gobies, small distinctive masses of cells associated with the ovarian wall develop into testis-associated glandular structures during sex change. These precursive accessory gonadal structures, or pAGS, have been found in females of known protogynous goby species, but not among gonochoric goby species, suggesting that their presence can be used as a species-specific indicator of protogyny within the family. However, a detailed examination of a developmental series of ovaries in two gonochoric species,Gobiosoma illecebrosum andG. saucrum, revealed the presence of a gonadal feature previously thought to be restricted to protogynous gobies. Among immature females of both species, pAGS-like structures having a similar appearance and placement as functional pAGS of protogynous gobies were found. In femaleG. illecebrosum, the size of these structures among immatures progressively decreased with maturation and were absent in all but the smallest adult females. A similar pattern was evident in a small sample ofG. saucrum. Population demography based on field collections showed thatG. illecebrosum exhibits sex ratios and male and female size-frequency distributions typical of gonochores and laboratory experiments indicated that final sexual identity was unaffected by social environment during the juvenile period. Thus, the presence of pAGS in juvenile femaleG. illecebrosum is not related to an ability to change sex at that ontogenic interval. Whether the transient pAGS observed here are vestiges of an ancestral protogynous condition is unknown. Based on their presence among immatures in two gonochore gobies, however, only the presence of pAGS in adult females should be used to predict protogyny among gobies.     

未产卵雌性黄鳝的性转变

为探讨产卵是否为雌性黄鳝(Monopterus albus Zuiew)性转变的必经过程, 研究分析了实验室内从受精卵或幼苗开始养殖至不同时间段的黄鳝性腺组织学状况, 采用性腺活检技术跟踪了34月龄雌性黄鳝性腺发育变化, 并以免疫组织化学方法探讨了黄鳝不同发育状态性腺中增殖细胞核抗原(PCNA)的分布。在养殖过程中, 实验黄鳝没有出现产卵现象或者繁殖行为。在5月龄黄鳝中, 间性占比13.3%, 雄性占比20.0%; 在12月龄(1龄)黄鳝中, 雄性占比17.6%; 34月龄(3龄)黄鳝中, 间性占比12.8%, 雄性占比8.5%。通过性腺活检技术对36条34月龄雌性黄鳝性腺发育变化进行了为期1个月的跟踪研究, 结果表明, 16.7%的雌性黄鳝发生了性转变, 性腺发育到间性阶段。黄鳝间性早期性腺生殖褶增厚, 部分细胞呈现明显PCNA免疫阳性, 包括间质细胞、精原细胞和初级精母细胞。上述结果提示, 产卵并非雌性黄鳝发生性转变的必经过程; 黄鳝性转变初期, 性腺结构变化包括生殖褶中间质细胞和精原细胞的发生和增殖。     

Female spawning migrations of the protogynous wrasse,Halichoeres marginatus

Spawning sites and spawning migration paths of tagged females of the protogynous wrasse,Halichoeres marginatus, were studied on the shallow reefs at Kuchierabu-jima Island, Japan. Males set up mating territories above prominent rocks on the offshore reef slope in the late afternoon, and pair-spawned with females, which had migrated there from their home ranges located in inshore areas. Small females migrated to the spawning sites near their home ranges, whereas large females migrated to various spawning sites located within a wide area, including downcurrent sites. Spawning at the downcurrent sites favors transport of eggs offshore, thereby increasing the female’s fitness. The spawning sites where an individual had spawned as a female were subsequently used for mating after it had changed sex. It is suggested that the wide migration of females to various spawning sites, enables the storing up of information on those sites, which later helps in the acquisition of mating territories after changing sex.     

Two alternative female tactics in the polygynous mating system of the threadsail filefish,Stephanolepis cirrhifer (Monacanthidae)

Reproductive behavior of the threadsail filefishStephanolepis cirrhifer was studied at Kashiwajima, southern Shikoku, Japan. This species spawned in pairs on the sandy bottom, the eggs being scattered over an area of about 15 cm in diameter and attached to sand particles. After spawning, males departed immediately, while the females remained at the site to guard the eggs for a few minutes. Thereafter the eggs were left unguarded for three days until hatching. Females spawned only once daily, whereas males mated with multiple females in succession. The reproductive males established territories, in which 1–4 resident females defended smaller territories from each other. The harem size changed according to some ecological conditions, such as population density. Moreover, the males also mated with visiting non-resident females. Thus, the two alternative tactics of females resulted in two mating patterns, haremic polygyny and female visiting of male territories, in a single population ofS. cirrhifer.     

Modeling spawning strategy for sex change under social control in haremic angelfishes

In haremic angelfishes where protogynous (female to male) sexchange is favored, females have been reported to adopt severaltactics for earlier sex change on the basis of a trade-offbetween reproduction and growth, or survivorship. A recentfield study on Centropyge ferrugatus revealed that femalesreduce spawning frequency in competition with similar-sized neighbors for social dominance. To evaluate the optimal spawningstrategy taken by haremic fishes, we developed an evolutionarilystable strategy model that focuses on their life history andsocial structure based on field data of C. ferrugatus. Theresults of the analysis predict that the spawning frequencywill be low when the mortality rate of females is high comparedwith males, the harem size is large, and there is a moderatedegree of social control. Our model further predicts conditionsunder which females completely stop spawning, as if they havebecome bachelors. Thus, the regulated spawning frequency maybe taken as a strategy to optimize the reproductive successof an individual in response to the available choices for sexchange, social control, and environmental conditions. Socialcontrol would also play an important role in sex change inmany other haremic species.