Japanese Journal of Ichthyology 魚 類 学 雑誌 、 Vol.24,No.21977 24巻2号1977年

Reproductive Behavior and Patterns of Sexuality in the Japanese Labrid Fish cupido

Katherine A.Meyer*

(Received January 25,1977)

Abstract The reproductive behavior and sexual organization of Thalassoma cupido(Tern- minck et Schlegel)were studied at the island of Miyake-jima,Japan,from June 1974 to

autumn of 1975.Spawning begins in mid-June,continuing until the middle of September, in sea temperatures ranging from 20.0•Ž-28.0•Ž.Spawning was observed only in the

morning,although was rarely seen in the afternoon. Of 195 specimens examined,52.8% were males,44.6% were females,while the remainder were undetermined.Both males and females have a wide size distribution,with males outnumbering females in the uppermost size range.Thalassoma cupido is a protogynous, diandric species.Initial and terminal color phases were noted.The initial phase includes juveniles,females,primary males,and secondary males.The terminal phase appears to be restricted to primary and secondary males. Both pair and aggregate spawning were observed,the latter more frequently in Miyake waters.Courtship and spawning behavior are described and compared with congeners.

The current literature contains considerable T.cupido(Temminck et Schlegel).Aggregate information on the reproductive behavior and spawning of T.lucasanum was described by sexual organization of members of the labrid Hobson(1965),and Randall and Randall(1963) genus Thalassoma Swainson.Various aspects briefly discussed monochromatism in T. of the reproductive behavior and biology of ballieui(Vaillant et Sauvage). the Atlantic species,T.bifasciatum(Bloch), Although Thalassoma cupido is one of the have been investigated independently by nu- most abundant fishes along the Pacific coast merous authors(Stoll,1955;Randall and of central Japan,no one has attempted to Randall,1963;Zumpe,1963;Feddern,1965; study the reproduction of this in detail. Reinboth,1967,1970,1972,1973,1975; Matsuoka(1972)reported a single observation Roede,1972;Warner et al.,1975;Robertson of aggregate spawning at Ryugu Island in a and Hoffman,in press;Warner and Robertson, short ecological note.Moyer(1974)described in press).The comprehensive study by Choat and discussed the reproductive behavior of T. (1969)on the biology of labroid fishes at cupido on the basis of observations made over Heron Island,Australia,includes information a five day period.To date,Reinboth(1975) on the sex structure of Thalassoma hardwickei has been the only person to examine the (Bennett),T.lutescens(Lay et Bennett),T. gonads of this species.In his small sample lunare(Linnaeus)and T.janseni(Bleeker). of nine specimens,he found no indication In a subsequent study,Robertson and Choat of spontaneous sex-inversion and stressed the (1974)provided further details on hermaphro- need for additional studies.Noting also that ditism in T.lunare,placing special emphasis dichromatism in the species had not been on social and systems.Reinboth(1962) recorded,he stated:"Further investigations originally reported on diandry in T.pavo are highly desirable since it appears some- (Linnaeus).In a compilation of data on 16 what irritating that Th.cupido should be labrid species,Reinboth(1975)summarized an exception within the genus Thalassoma his findings on the sexual organization of T. with regard to its uniform coloration and its pavo,T.lucasanum(Gill),T.bifasciatum and eventual gonochorism." * Present address:2701 Dauphine,New Orle - This paper deals principally with the sexual ans,Louisiana 70117,U.S.A. behavior of Thalassoma cupido and provides

―101― 魚 類 学 雑 誌Japan.J.Ichthyo1.24(2),1977 additional information on the reproductive volcanic rocks and boulders,covered primarily ecology and physiology of the species.The with the brown alga Sargassum,a high diver- occurrence of sex-inversion is reported and sity of fleshy and filamentous red algae,and sexual dichromatism is described for the first intermittent growths of coral.The flow of time. a weak current can occasionally be felt as it passes through the spawning site. Materials and methods There is some evidence to suggest that the The reproduction of Thalassoma cupido was depth at which spawning takes place varies studied at Miyake-jima(34•‹5'N,139•‹30'E), with different size groups.Small adults show- one of the Izu Islands of Japan.Using ed little preference for depth,whereas larger SCUBA,daily observations were made from fish appeared to be more selective.Fish of June through September of 1974 and 1975, all sizes,including some as small as 50 mm with less intensive studies continued through- TL,were commonly seen in spawning aggre- out the remainder of each year.Field obser- gates at the site described above.Aggregates vations were supplemented with aquarium ob- observed at depths of less than 7 m consisted servations.Specimens used for this purpose primarily of fish in the lower size range.- were placed in a 158 1 aquarium,illuminated ing was observed in water as shallow as 1 m. by natural sunlight shining through two large b.The spawning season glass doors adjacent to the tank.Water The spawning season of T.cupido at temperature was maintained at approximately Miyake-jima is restricted to a period of ap- 28.0•‹C.Spawnings by captive fish were ob- proximately three months,beginning in June served on two occasions. and ending in September.The first spawning Intermittent collections of specimens were observed in 1974,was on June 17.As dives made throughout the study period for exami- were not made previous to this date,it can- nation of their gonads.A variety of methods not be stated whether this was in fact the was employed in collecting these specimens, first spawning of the year.However,the including hook and line,fish trap,spear,and following year,the spawning site was visited screen net.Collections were made at a num- daily for some time before spawning was first ber of locations around the island.A total observed,again on June 17.Reproductive of 220 specimens were dissected and selected activity was noted for the last time on Sept- gonads were prepared for histological sections. ember 15,in 1974,and on September 10,in 10% formalin was used for fixation.The 1975.These dates did not correspond in gonads were sectioned at 7 p and stained with either year to marked changes in temperature haematoxylin and eosin. or photoperiod. Specimens selectively collected from spawn- c.Diurnal periodicity in spawning ing aggregates are excluded in the sex ratio Reproductive activity in Igaya Bay occurred and related figures. only during a period of several hours in the morning from about 0830 to 1200.On dives Results made before 0800,very few were Reproductive activity as related to environ- found at the spawning site.Solitary fish mental factors began to appear around 0700.Between 0800 a.The spawning grounds and 0830 the formation of aggregates began and Observations of spawning were focused in pre-spawning or courtship behavior could be Igaya Bay,on the west side of the island. observed.The number of fish at the spawning Although reproductive activity was noted at site decreased noticeably between 1100 and various locations in the bay,it was consist- 1200;the latest observed spawning occurred ently found to be highly concentrated at one at 1215.On rare occasions courtship behavior area,about 150 m offshore.This spawning was noted in the afternoon,although subse- site encompasses an area of approximately quent spawning acts were not observed. 1460 m2,ranging in depth from 9 to 11.5 m. However,Mr.Y.Yogo(personal communica- The bottom consists of sand with overlying tion)has witnessed mid-afternoon spawnings

―102― Meyer:Reproductive Behavior and Patterns of Sexuality of a Labrid Fish by this species at Amakusa,Kyushu,on at spection .Both males and females had a wide least two occasions.At Miyake-jima no cor- distribution in terms of size,maintaining a relation was found between the timing of ratio which closely approximated unity reproductive activities and the daily tidal throughout most of the size range.However, rhythm. among the largest specimens,males heavily d.The influence of temperature outnumbered females(Fig.1). Spawning was observed at water tempera- c.Diandry tures of 20.0•Ž to 28.0•Ž.Reproduction did Thalassoma cupido is a diandric species,its not occur on the few days when the tem- males having two types of ontogenetically, perature fell below 20.0•Ž,suggesting that and thus morphologically,distinct testes.As low temperatures inhibit reproductive activity. Yet the overall influence of temperature dur- ing the spawning season is probably slight, as periods of cold sufficient to inhibit spawn- ing are minimal at this time.Temperature during the spawning season of 1974 ranged from 19.0•Ž to 27.5•Ž but averaged a mod- erate 23.3•Ž.The 1975 temperature range during the spawning season was 16.0•Ž to 28.0•Ž,averaging 24.8•Ž. e.The influence of heavy rainfall Frequently,spawning was not observed dur- ing and soon after periods of heavy rainfall. Such weather conditions resulted in an ap- preciable amount of silt and freshwater run- off from the cliffs surrounding the bay.Heavy overcast in combination with turbid waters noticeably reduced the visibility,on occasion making field observations difficult or impos- Fig.1.Size and color distribution as related to sible.Whether the lack of spawning observ- sex of Thalassoma cupido collected at Miyake- ed during heavy rains was a direct response to jima.• ^,Initial color phase;• ,interme- such conditions remains uncertain.An in- diate color phase;• ,terminal color phase. triguing question is whether mating fish are negatively influenced by chemical alterations Table 1.Color,size,and sexual derivation of the water which might affect the viability of 13 male specimens of Thalassoma of freshly fertilized eggs. cupido.

Reproductive physiology

a.Size at sexual maturity The smallest mature female collected was a 42 mm SL specimen containing fully devel- oped ovaries with ripe eggs.The smallest mature male specimen measured 44 mm SL. Spawning aggregates comprised exclusively of these very small adults were occasionally en- countered. b.Sex ratio Of 195 specimens examined,103(52.8%) were found to be males,87(44.6%)were females and the sex of 5 specimens(2.6%) could not be determined by macroscopic in-

―103― 魚 類 学 雑 誌Japa11.J.Ichthyol.24(2),1977

Fig.2.Cross sections of primary testis(A)and secondary testis(B)of Thalassoma cupido. fw,former ovarian wall;vd,vas deferens.Photos by Dr.A.Nakazono. shown in Table 1,histological examination porarily broken into two series of quadrate of 13 testes revealed ten primary testes and dark blotches,or they may become very dark, three secondary testes(Fig.2).In the latter, appearing as two distinct black bands.A the testicular lobes are surrounded by a thin third narrower longitudinal band runs back- membrane derived from the ovarian wall. ward from the lower pectoral base,becoming The vas deferens develops as a ramified sys- somewhat faded posteriorly.The head and tem within this membrane.In contrast,the median fins are also green with brick-red primary testes have a cylindrical vas deferens markings.A prominent black blotch covers between the right and left lobes.Further the second interspinous membrane of the evidence for the ovarian origin of secondary dorsal fin.The thorax and abdomen are gonads lies in the arrangement of the testi- pale blue.The ventral and pectoral fins are cular tissue,which surrounds the former hyaline,the latter with blackish tips.The ovarian cavity.Cross sections of the primary intensity of this black coloration varies con- and secondary testes of this species are shown siderably,fading and darkening within sec- in Fig.2. onds. The color phase described above is most Sexual dichromatism prevalent among fish in the lower size ranges Two color phases are found among the (Fig.1)but has a wide distribution in terms adults of Thalassoma cupido.While not sharp- of sexual identity;it is found among juveniles. ly contrasting,these color phases are never- females,primary males,and secondary males. theless clearly distinct.Characteristic of the The two secondary males which were found more common form is the prevailing green among specimens included in this color group coloration.Running along the entire body were fully transformed,functional males. length are two broad,brick-red,irregular, This form will subsequently be referred to as longitudinal bands.These bands may he tern- the"initial"color phase in accordance with

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the terminology proposed by Reinboth(1975). comprise as many as 150 individuals.Collec- A small minority of fish(estimated to be tions from among spawning aggregates re- less than 1% of the population)undergo a vealed a heavy preponderance of males.In color transformation to the"terminal"color one aggregate of 14 fish,4 fish proved to be phase.This is achieved primarily by a change females and in another aggregate of 11 fish, in the green pigmentation.The ground color only one female was found. of the head,the body,and median fins change The groups observed at the spawning site from green to deep blue.The pectoral fins may be best described as loose aggregations assume a blue tinge,while the thorax and of milling fish.The aggregating fish swim abdomen darken their original blue color. an irregular path,frequently changing direction Color transformation,however,is not accom- so that individual members of ten vary in their panied by the disappearance of existing mark- orientation.The characteristic motor pattern ings or the addition of new traits.The final among these fish is a peculiar bobbing motion impression is that of a brightly colored,pre- in which the entire body is moved steadily dominantly blue fish,as opposed to the drab up and down by simultaneous vertical strokes greenish coloration peculiar to the initial of the pectoral fins.Bobbing fish swim slowly, phase.The terminal phase was found only sometimes barely moving forward at all,and among large adult males(Fig.1).Because often brush against the bodies of others swim- fish with this color pattern are scarce,the ming below or nearby.Also characteristic of sample size is correspondingly small.However, aggregate members is a uniform change in the sexual behavior of other terminal phase coloration,typified by a darkening of the two fish observed in the field strongly suggests that broad longitudinal bands on the body which all are males.These may be either primary appear as dominant features. or secondary in derivation. Spawning aggregates are not always well- Individuals with an intermediate color pat- defined,isolated entities;aggregates may tern were often observed underwater.How- merge with neighboring groups or may break ever,in the sample obtained there were only into yet smaller units.In addition to fre- three such specimens.All of these proved quent departures and the arrival of new fish, to be primary males. mild chases contribute to the unstable nature of the aggregations.Most groups contain a Reproductive behavior single individual that behaves quite differently In common with many labroid fishes, towards the other aggregate members,often Thalassoma cupido exhibits both pair and treating them aggressively.These individuals aggregate spawning(Randall and Randall, are positioned at the periphery of the aggrega- 1963).Groups comprising only initial phase tion and have a greater range of movements, fish engage in aggregate spawning.Pair swimming around and above the others.They spawning is performed by a terminal phase exhibit individualistic behavior,typified by male and an initial phase female or,more more forceful movements and a distinctive rarely,by two initial phase fish.Males dis- manner of swimming whereby the pectoral playing an intermediate color pattern also fins are fluttered rapidly,conspicuously dis- participate in pair spawning activities.Ag- playing their blackened tips.Despite their gregate spawning is the preponderant type in unique prespawning behavior,these fish nor- the waters around Miyake-jima and may be mally participate in the spawning act in a readily observed on most days during the manner identical to that of the other group spawning season.Pair spawning is conspicu- members. ously less common. Occasionally,more highly organized groups a.Aggregate spawning may be observed,in which the fish are simi- During periods of reproductive activity, larly orientated,swim at a uniform pace,and large numbers of T.cupido gather in groups exhibit coordinated movements.In these of varying sizes at the spawning site.It is groups,the foremost position is maintained by estimated that the largest of these groups a single fish which appears to lead the others.

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Spawning in the milling aggregations is pre- back and forth or in a roughly circular path ceded by greater cohesiveness and uniformity above the female,propelled primarily by a of movements.Immediately prior to spawn- rapid fluttering of the pectoral fins.After ing,three or more fish abruptly break away a series of such circuits,he dips downward from the aggregation,move forward with ac- as he approaches the female so that he is celerated fin movements,and come together positioned directly above her.This downward in a tight group,tilting their bodies upward movement is accompanied by an acceleration in a diagonal position.Sometimes this abrupt of pectoral fin fluttering and the onset of a forward movement is repeated several times high speed beating of the caudal fin,a com- in rapid succession.The upward spawning bination which creates an impression of the dash then follows,the apex at which the eggs entire body quivering.Continuing this dis- and sperm are released.The height of the play,the male hovers a few centimeters above upward dash varies considerably,from a mini- the female for several seconds,his body vari- mum of approximately 13 cm to a maximum ously positioned in a lateral arch(Fig.3,A) of about 1.5 m.Immediately after spawning, or slanted slightly upwards(Fig.3,B).When the fish move slightly apart and swim down- in the former position,he may turn tight wards with great rapidity.The wrasses may semicircles around the female,displaying alter- reassemble upon returning to the bottom or nately to her left and right sides. they may disperse.The entire spawning se- If the female is not immediately receptive, quence occurs within the span of about one the male will resume his original position and second. repeat the entire sequence.Most often the b.Pair spawning is repeated a number of times before Mating pairs are temporary associations, the female responds.Usually she lies nearly enduring for only the short period of fertili- motionless in the algae with only her head zation.Pair formation begins when the male protruding until emerging to spawn.As in encounters a female or isolates one by chasing aggregate spawning,the pair dash rapidly up- and driving her into the algae.A conspicu- ward,usually about 25-50 cm,where the ous courtship display follows.Although the eggs and milt are released.The cloud of courtship sequence is not entirely rigid,it reproductive material is less obvious than nevertheless has a characteristic pattern which that observed during aggregate spawning. can be described as follows:the male swims The female appears to initiate the upward

(A) (B) Fig.3.Variations of the courtship display performed by pair spawning males of Thalassoma cupido.See text for details.

―106― Meyer:Reproductive Behavior and Patterns of Sexuality of a Labrid Fish dash.During the onset she holds the leading by the juvenile damselfish,Dascyllus position,with the male following closely be- reticulatus(Richardson),was also observed. hind. Matsuoka(1972)reported an observation of Rarely,pair spawning is not preceded by T.cupido feeding on the fresh spawn of con- the typical courtship display.In these in- specifics in the sea.However,this probably stances,the male vigorously chases the female. occurs only rarely as I have never witnessed The chase terminates when the female abrupt- such behavior in the field. ly ceases to flee,and spawning immediately Mating fish are also vulnerable to predation. follows. The large concentrations of fish in spawning During periods of reproductive activity,in- aggregations and conspicuous sexual displays dividually recognized pair spawning males were of this species seemed to attract predators to found daily at the spawning site.Although the spawning site.The lizardfish Synodus these males roam widely,familiarity with variegatus(Lacepede)was the most common individual fish revealed that select areas were of these predators.On at least 30 occasions, visited repeatedly and occupied for lengthy. this lizardfish was observed to attack with periods of time.These areas are usually situ- great speed just as the wrasses formed the ated immediately within the aggregate spawn- characteristic close-knit group immediately ing grounds or in close proximity.Often prior to the upward dash.Similar attacks by they are located along the outskirts.These S.variegatus,directed at pair spawning fish, areas lack rigid boundaries but usually cover were also frequently observed.The serranid a distance of about 6-10 m2.Generally they Epinephelus fasciatus(Forsskal)also appeared surround some natural landmark of notable to show interest in the spawning aggregations stature.Spawnings by such pair spawning (Moyer,personal communication).Other suc- males are largely restricted to these sites. cessful predators were Muraena pardalis Tem- The male dominates the area during his pre- minck et Schlegel and an unidentified scor- sence,actively chasing away some conspe- paenid.When attacked,the wrasses quickly cifics.The tolerance with which other con- dispersed,seeking refuge under the algae specifics are treated upon intrusion suggests where they remained for about 30 seconds. that territories are defended against competi- tive males only,in defense of potential spawn- Discussion ing partners.Fish that are not attacked ap- a.Sex-inversion parently pose no threat to the reproductive It is well known that protogynous sex-inver- success of the male.Agonistic interspecific sion is common among labrid fishes.Within encounters were never witnessed. the family Labridae,protogyny is expressed in a variety of forms,from species in which Response of predators to reproductive all males are derived secondarily from females, activities to species in which varying numbers of in- Five species of pomacentrid fishes,Poma- dividuals are born as males and never undergo centrus coelestis Jordan et Starks,P.nagasaki- a sex change.Reinboth(1975)has emphasiz- ensis Tanaka,Chromis flavomaculata Kamo- ed the extreme variability which exists be- hara,C.chrysura(Bliss),and C.miyakeensis tween protogynous wrasses in regards to the Moyer et Ida,regularly fed on the pelagic particulars of sex and color transformation eggs of this species.These damselfishes gath- and their interrelationships.His data indicate ered above the spawning aggregations and ate differences even among congeneric species. the eggs as soon as they were released.Egg Table 2 provides a comparative summary of predation by these fishes has been described some pertinent information currently available in greater detail by Moyer(1975).In addition on members of the genus Thalassoma for to the above,I once also witnessed the anem- which protogynous sex-inversion has been onefish Amphiprion clarkii(Bennett)feeding demonstrated. on eggs released by the wrasses just outside An outstanding feature of protogynous her- of the host anemone.In the aquarium,egg maphroditism in Miyake-jima populations of

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Table 2.Summary of selected information on sex and color schemes for protogynous species

of the genus Thalassoma.Sources are given in parenthesis:1,Choat(1969);2, Kuhn(1976);3,Reinboth(1962);4,Reinboth(1967);5,Reinboth(1970);6,Rein-

both(1972);7,Reinboth(1973);8,Reinboth(1975);9,Robertson and Choat(1974); 10,Roede(1972);11,Stoll(1955);12,Warner and Robertson(in press);13,Present

study.*,no distinction made between primary(1•‹)and secondary males(2•‹). Data listed under the headings"initial color phase"and"terminal color phase"are derived only from the samples examined by the authors cited and may,in some

cases,be incomplete.

Thalassoma cupido is that the secondary male number of females was significantly higher component appears to be very small.Even than that of males.Choat(1969)obtained in those species in which primary males con- similar results in his survey of labrid fishes tribute significantly to the population,the at Heron Island,Australia.That a biased protogynous state is often reflected in unequal sex ratio is evident in T.cupido only in the sex ratios and an unbalanced distribution of uppermost size range suggests that most males the sexes with size.For example,in a study enter the population during juvenile stages. of seven protogynous labrid species from the Though limited,histological investigations ,Roede(1972)found that in every provided further evidence for the paucity of species females prevailed at small sizes,while secondary males in this species.Although males predominated at large sizes.Further- 23% of the specimens examined histologically more,in six of the seven species,the total were secondary males,these specimens were

―108― Meyer:Reproductive Behavior and Patterns of Sexuality of a Labrid Fish intentionally selected on the basis of their coloration,and an active role of males in large size,and in some cases,their interme- courtship activities.Females,on the other diate or terminal color pattern in order to hand,lack a special sexual color pattern and obtain a sample which one would expect to well-developed sexual displays,and play a be biased towards sex-inversed males.Taking quiescent role in courtship.This scheme is into account this biased method of sampling, also well suited to the mating systems of secondary males would seem to be very scarce. T.lunare(see Robertson and Choat,1974)and Recent studies(Warner et al.,1975;Warner T.cupido.It should be added that basic to and Robertson,in press)have shown that in this system is the existence of two differing Thalassoma bifasciatum the proportionate modes of reproduction;aggregate and pair number of primary males varies in popula- spawning. tions of different sizes;they are common in In pair spawning,transient mating pairs large populations and rare in small ones.It are formed which endure for only the short has been suggested that this is the result of period of fertilization.Hence,males mate selective pressures against initial phase males, promiscuously with many females.In each and thus primary males,in small populations species,pair spawning males hold temporary where terminal phase males are better able territories during periods of reproductive ac- to control the entire spawning area and ef- tivity which they defend from other males fectively reduce the spawning activity of ini- and in which they perform sexual displays tial phase males.How these and other factors and fertilize the eggs of individual females. might interact in determining the relative In a comparative analysis of courtship pat- number of primary and secondary males in terns in three species of tropical labrids T.cupido requires further study to explain (Clepticus parrae,Labroides dimidiatus,and the apparent scarcity of secondary males in Thalassoma bifasciatum),Robertson and Hoff- Miyake-jima populations.The physiological man(in press)and Robertson(personal com- process of sex-inversion in this species also munication)distinguished two types of sexual deserves further -attention and an extensive displays;long distance communicative dis- histological survey is needed. plays and short distance displays.For ex- b.Comparison of reproductive behavior ample,in T.bifasciatum"loopings"(Rein- with congeneric species both,1973)are performed even in the absence A high degree of similarity is found in com- of females and apparently serve to announce paring the sexual behavior of Thalassoma the presence and location of the territorial cupido with that of T.lunare and T.bifasci- male.Supplementary to looping is a series atum,the two congeneric species for which of close proximity activities which a male detailed studies have been made. directs to an approaching female as he circles A basic characteristic common to these above her.These displays consist primarily three species is the existence of a loosely of pectoral fin fluttering and tail quivering. organized social system in which permanent Robertson and Choat(1974)described simi- dominance relationships are lacking,thus lar close proximity displays for terminal phase denying males direct access to and control males of T.lunare,but gave no account of over females.This is in contrast to the sys- long range displays analogous to looping. tem seen in Labroides dimidiatus(Valencien- Similarly,only close proximity displays were nes),in which harems are established and a observed of T.cupido.These displays are rigid hierarchy is maintained based on the directed towards isolated individuals,clearly dominance of a single male over a group of serving a courtship function.In common females(Robertson and Choat,1974).Ro- with T.bifasciatum and T.lunare,pectoral bertson and Hoffman(in press)have sug- fin fluttering and tail beating are the basic gested that,in T.bifasciatum,free female motor patterns of the courtship display. and the need for males to com- Because territories are so poorly defined,it pete for spawnings has led to the develop- is difficult to ascertain the relative extent to ment of specific male sexual displays and which males of each species are active in

―109― 魚 類 学 雑 誌Japan.J.Ichthyo1.24(2),1977 searching for and procuring their spawning the other was rare,a factor which Hubbs partners.It appears,however,that the lack (1961)suggests may contribute to the break- of long range announcement displays in T. down of barriers to interbreeding.Although cupido is compensated for by a more active these are clearly exceptional cases,they provide role on the part of pair spawning males in additional evidence that among members of selecting mates.Female T.bifasciatum come the genus there exists a high degree of con- to the male's territory when ready to spawn, formity in patterns of reproductive behavior. often waiting there if the male is absent or c.The frequency of aggregate and pair preoccupied(Reinboth,1973;Warner et al., spawning 1975).This was very rarely observed of T. Reinboth(1973)noted that in T.bifasciatum cupido.More often a male would be forced the relative frequency of aggregate spawning to stray to the outskirts of his comparatively and pair spawning varies at reefs of different large territory(roughly 6-10 m2,as opposed sizes;aggregate spawning seems to prevail on to the estimated 1 •`4 m2 reported for T. large reefs,while pair spawning prevails on bifasciatum),and intercept females from pas- small reefs.He speculated that,"pair spawn- sing aggregations.Frequently,a male would ing is the most efficient way of reproduction spend as long as 20 minutes driving off other in cases where equal physiological readiness males while attempting to isolate a female. may hardly be attained simultaneously by a In addition to T.bifasciatum and T.lunare, number of individuals".These requirements aggregate spawning has been reported for T. of synchronization are probably satisfied by hardwickei(Choat,1969)and T.lucasanum the short breeding season and extreme abund- (Hobson,1965).The spawning sequence as ance of T.cupido at Miyake-jima and may described for these four species does not differ contribute to the fact that aggregate spawning significantly from that of T.cupido.A single greatly exceeds pair spawning in frequency. exception is that"bobbing",which appears to d.The relationship between dichromatism be an important action pattern in T.cupido, and sexual behavior has not been previously noted in the literature. Previous investigators have found a direct The many similarities in sexual behavior correlation between male dichromatism and among these congeneric species may have sexual behavior among members of the ge- facilitated an incidence of interspecific spawn- nus Thalassoma.Initial phase males of T. ing observed during the course of this study. bifasciatum,T.lunare,and T.lucasanum nor- In July of 1975 pair spawning was seen be- mally spawn in aggregates while terminal tween T.cupido and its congener,T.lunare. phase males pair spawn.Occasionally spawn- Spawning proceeded in a manner typical of ing aggregations of T.lucasanum are joined. what has been described in this paper and by individuals clearly transitional to the ter- was preceded by the courtship display perform- minal male form and rarely by some that ed by the former species,a male in the terminal appear to have attained this form(Hobson, color phase.The isolated T.lunare was parti- personal communication).However,aggre- ally concealed in the seaweed and behaved in gate spawning by terminal phase T.bifasciatum a manner identical to that of female T.cupido and T.lunare appears to be quite rare,as prior to spawning.No other T.lunare were few examples of such spawnings have been seen in the vicinity.Although their patterns reported in the extensive literature on this differ,the blue coloration of terminal phase subject.Occasionally,initial phase males of T.cupido is very similar to that of T.lunare these two species will participate in pair and this may have also contributed to this spawning activities,although this occurs in a unusual spawning. rather peculiar fashion.An unusual trio is Subsequent to this observation another report formed as a second male rushes up to join a (Randall,1972)was discovered in which brief pair just as gametes are being shed(Warner mention was made of spawning between two et al.,1975).Initial phase males of T. species of Thalassoma.In both of these bifasciatum may also engage in pair spawn- instances,one species was very abundant while ing activities by"sneaking"(Warner et al.,

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1975).These fish approach the territory of among pair spawning males.Although color a sexually active terminal phase male and is a more reliable index of a male's spawn- induce spawning with individual females that ing strategy,this relationship is not absolute. are waiting to mate with the courting terri- It is suggested that the large size and bright tory holder. colors of terminal phase males confer an ad- The relationship between color and spawn- vantage in pair formation,normally to the ing behavior in Thalassoma cupido is similar exclusion of neighboring initial phase males. to that of its congeners.Aggregate spawning Yet under favorable conditions,initial phase by a terminal phase T.cupido was witnessed males will also compete for access to single only once throughout the several hundred ob- females. servations made.Participation in pair spawn-

ing by initial phase males of this species is Acknowledgments not restricted to trio formation,although this I am indebted to Dr.Akinobu Nakazono of behavior was rarely observed.On several occasions,typical pair spawnings were seen the Fishery Research Laboratory,Kyushu Uni- in which both participants were initial phase versity,for his extensive assistance in the fish.Perhaps some of these observations can histological investigations of gonad samples, be attributed to poor synchronization on the and for providing many helpful comments and suggestions throughout this study.Mr.Yutaka part of a small group,as was clearly the case when this was seen in the aquarium.How- Yogo of the Fishery Research Laboratory, ever,this is not always the case,as is evi- Kyushu University,Dr.Edmund S.Hobson of denced by occasional initial phase males which the Southwest Fisheries Center Tiburon Lab- actively pursue,court,and spawn with single oratory,Dr.D.Ross Robertson of the Smithso- females.These males behave in a manner nian Tropical Research Institute,and Prof. indistinguishable from that of terminal phase Rudolf Reinboth of the Institut Mr Zoologie, males,even defending territories for short Johannes Gutenberg-Universitat,are thanked for sharing valuable observations and infor- periods of time.Pair spawnings by such ini- tial phase males are not directly comparable to mation.Further thanks are due to Dr. the spawnings which result from "sneaking" Robertson for providing two of his unpublished in T.bifasciatum.They may take place in manuscripts.The assistance of Dr.Torao Sato areas removed from the territories of terminal of Tokyo University in locating pertinent literature,and that of Peter A.Hofmann in phase males and often do not involve inter- fering with the activity of terminal phase translating German articles is gratefully ac- territory owners. knowledged.Jennifer A.Crooks kindly pre- The most interesting example of this was pared the drawings of Fig.3.Dr.K.Mashiko the case of an exceptionally large initial phase of Teikyo University,Prof.Reinboth,Dr. fish which was observed daily throughout the Robertson,Dr.Nakazono,and Mr.Yogo 1975 spawning season engaged in reproductive are thanked for critically reading the manu- activity characteristic of terminal phase males. script.Finally,I wish to express my grati- Pair spawning by this individual was usually tude to Jack T.Moyer,John W.Shepard, observed several times each day.This was and Claire E.Sawyers,of the Tanaka thought to be its sole mode of reproduction Memorial Biological Station,who contributed. until once,when minutes after pair spawning, many valuable observations,ideas,and sug- it joined and spawned with an aggregate. gestions,assisted in collecting specimens,and Such observations indicate that initial phase provided encouragement and support. males possess a versatility in mating systems and that sexual behavior is not fixed,but is Literature cited variable depending upon the immediate social Choat, J. H. 1969. Studies on the biology of pressures.Sexual origins appear to have little, labroid fishes (Labridae and Scaridae) at Heron if any,influence over spawning behavior as Island, Great Barrier Reef. Pt.1. both primary and secondary testes were found and reproductive biology. Ph. D. Thesis, Univ.

―111― 魚 類 学 雑 誌Japan.J.Ichthyo1.24(2),1977

Queensland : 1 •`294. unters., 24: 174•`191, figs. 1•`5. eddern, H. A. F1965. The spawning, growth, and Reinboth, R. 1975. Spontaneous and hormone-

general behavior of the bluehead wrasse, Tha- induced sex-inversion in wrasses (Labridae). lassoma bifasciatum (Pisces: Labridae). Bull. Pubbl. Staz. Zool. Napoli, Suppl., 39: 550-573, mar. Sci., 15 (4): 896'-'941, figs. 1 •` 33. figs. 1•`8.

Hobson, E. S. 1965. Diurnal-nocturnal activity of Robertson, D. R. and J. H. Choat. 1974. Proto- some inshore fishes in the Gulf of California. gynous hermaphroditism and social systems in Copeia, 1965 (3) : 291-302, 1 fig. labrid fish. Proc. Int. Symp. 2nd.,

Hubbs, C. L. 1961. Isolating mechanisms in the 1: 217-225, figs. 1•`4. speciation of fishes. Univ. Texas. Symp., Ver- Robertson, D. R. and S. G. Hoffman. (In press).

tebrate Speciation: 5•`23. The role of female mate choice and predation Kuhn, R. 1976. Morphologische und histolo- in the mating systems of tropical labroid fishes.

gische Untersuchungen zum Geschlechtswechsel Roede, M. J. 1972. Color as related to size, von Thalassoma pavo (L.), einem diandrisch sex, and behavior in seven Caribbean labrid

protogynen Lippfisch aus dem Mittelmeer. Ph, fish species (genera Thalassoma, Halichoeres and D. Thesis, Univ. Mainz. (not seen ; personal Hemipteronotus). Studies on the Fauna of

communication from R. Reinboth). Curacao and other Caribbean Islands, 42: 1 •` Matsuoka, T. 1972. The fishes found in the 266, figs. 1•`25, pls. 1•`11. rocky shore of Shirahama, Ryugu-jima, Shimoda Stoll, L. M. 1955. Hormonal control of the

and adjacent waters. Bull. Shizuoka Pref. Fish. sexually dimorphic pigmentation of Thalassoma Exp. Stat., 5: 89•`111, figs. 1•`2, pls. 1•`5. bifasciatum. Zoologica, 40 (11): 125-132, pls.

Moyer, J. T. 1974. Notes on the reproductive 1•`3. behavior of the wrasse Thalassoma cupido. Jap. Warner, R. R. and D. R. Robertson. (In press).

J. Ichthyol., 21 (1): 34•`36. Sexual patterns in the labroid fishes of the Moyer, J. T. 1975. Reproductive behavior of Western Caribbean : I. The wrasses (Labridae).

the damselfish Pomacentrus nagasakiensis at Warner, R. R., D. R. Robertson, and E. G. Leigh,

Miyake-jima, Japan. Jap. J. Ichthyol., 22 (3) : Jr. 1975. Sex change and . 151-163, figs. 1•`5. Science, 190 (4215): 633-638, 1 fig.

Randall, J. E. 1972. A revision of the labrid Zumpe, D. 1963. Ober das Ablaichen von Tha- fish genus Anampses. Micronesica, 8 (1•`2) : lassoma bifasciatum. Dt. Aquar. Terrar. Z., 16: 151-195, figs. 1•`10, pls. 1•`3. 86-88. (not seen.) Randall, J. E. and H. A. Randall. 1963. The

spawning and early development of the Atlantic (Tatsuo Tanaka Memorial Biological Station, Ako, Miyake-jima, Tokyo 100-12, Japan) parrot fish, Sparisoma rubripinne, with notes on other scarid and labrid fishes. Zoologica,

48 (5): 49•`60, figs. 1•`2, pls. 1•`2. ニ シ キ ベ ラ の 一 次 雄,二 次 雄 に お け る 性 徴 と 生 殖 行 動 Reinboth, R. 1962. Morphologische und funk- Katherine A.Meyer tionelle Zweigeschlechtlichkeit bei marinen Teleostiern (Serranidae, Sparidae, Centracan- 三 宅 島 に お い て1974年6月 か ら1975年 秋 に か け

thidae, Labridae). Zool. Jb. Physiol, 69: 405 •` て,ニ シ キ・ベ ラ の 生 殖 行 動 と性 構 造 を 観 察 し た.産 卵 480, figs. 1•`37. は6月 中 旬 か ら9.月 中 旬 ま で 続 き,そ の 間 の 水 温 は

Reinboth, R. 1967. Biandric teleost species. 20.0～28.0℃ で あ っ た 。 求 愛 行 動 は ま れ に 午 後 に 観

Gen. comp. Endocr., 9 (3) : abstr. no. 146. 察 さ れ る こ と も あ る が,産 卵 は 午 前 だ け に 限 ら れ た 。 Reinboth, R. 1970. Intersexuality in fishes. In 195尾 の 調 査 個 体 の う ち,52.8%は 雄,44.6%は 雌 Hormones and the environment. Mem. Soc. (残 り は 不 明)で あ っ た.雌 雄 と も に 同 範 囲 の 体 長 分 布

Endocr., 18: 515-543, figs. 1•`2, 1 tb., pls. 1•`2. を 示 し た が,そ の う ち 特 に 大 型 の 個 体 に つ い て だ け み

Reinboth, R. 1972. Some remarks on secondary れ ば,雄 の 数 は 雌 よ り多 い 。 本 種 は 雌 性 先 熟 現 象 に よ sex characters, sex and sexual behavior in り雄 に2型 を 示 す 。 体 色 相 の 変 異 に つ い て も観 察 し,

teleosts. Gen. comp. Endocr., Suppl., 3 : 565 initial phaseは 未 成 魚,雌,一 次 雄,二 次 雄 に 認 め ら 570, 1 fig. れ る が,terminal phaseは 一 次 雄,二 次 雄 に 限 ら れ

Reinboth, R. 1973. Dualistic reproductive be- る 。 ペ ァ 形 成 産 卵 と群 れ 形 成 産 卵 の 両 型 が観 察 さ れ た havior in the protogynous wrasse Thalassoma が,本 研 究 水 域 で は 後 者 が よ り頻 繁 で あ っ た 。 求 愛 行

bifasciatum and some observations on its day- 動 お よ び 産 卵 行 動 の 記 載 を 行 な い,同 属 の 他 の 魚 種 と night changeover. Helgolander wiss. Meers- の 比 較 検 討 を 行 な っ た 。

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