Reproductive Behavior of the Damselfish Pomacentrus Nagasakiensis at Miyake-Jima,Japan

Japanese Journal of Ichthyolog y 魚 類 学 雑 誌22巻3号 Vol.22,No.31975 1975年

Reproductive Behavior of the Damselfish Pomacentrus nagasakiensis at Miyake-jima,Japan

Jack T.Moyer

(Received February 15,1975)

Abstract The reproductive behavior of Pomacentrus nagasakiensis Tanaka was studied on the island of Miyake-jima,Japan,from July 1973 to October 1975.Reproductive activity began in May,when water temperatures reached 22°C and continued until early September.The heaviest concentrations of reproductive activity coincided with the waxing of the moon, reaching a peak 2 3 days prior to the full moon. Like other pomacentrids,males construct and guard nests.Smooth sides of boulders or discarded pots,pipes,tires,etc.are used as nesting surfaces.Females are attracted with typical pomacentrid "signal jumps".Females are led to nests by an enticement display,which is clearly a distinctive action pattern from the signal jump.Spawning usually occurs in early morning or late afternoon.Several thousand eggs are laid in a single spawning.The male guards the nest and fans the eggs.Typically,a male may guard about ten patches of eggs in a season.Spawning with two or three females may occur within a few days,and a single male may care for three clutches of eggs in a single egg patch. Males with nests in favorable locations defend their territories persistently throughout the breeding season.Territories in less favorable locations are defended only during periods of active spawning. The following motor patterns are recognized for P.nagasakiensis during the courtship phase of reproduction:signal jumps,enticement,chasing,and skimming.

(Jordan and Evermann),Matsuoka(1962,1972) Introduction reported certain aspects of the reproductive Since the late 1950s,when SCUBA became behavior of P.coelestis Jordan and Starks,and an indispensable aid to marine research,the Honda and Imai(1973)studied breeding and family Pomacentridae has received considerable development of Pomacentrus nagasakiensis Ta- attention as an outstanding subject for etholo- naka in the aquarium.Breder and Coates(1933) gical research.The genus Chromis Cuvier has and Brinley(1939)reported on aquarium ob- been an especially popular subject for study, servations of spawning and egg development with many papers appearing on various aspects in two species of the closely related genus of behavior(Abel,1961;Albrecht,1969;Fish- Eupomacentrus Bleeker. elson,et al.,1974;Limbaugh,1964;Myrberg, The reproductive behavior of the damselfish, et al.,1967;Sale,1971;Swerdloff,1970 a,b). Pomacentrus nagasakiensis was studied near the These studies have resulted in a growing knowl- Tanaka Memorial Biological Station(TMBS) edge of phylogenetic relationships within this on the offshore Japanese island of Miyake genus. (34°5'N,139°30'E)from July 1973 to October It is rather surprising that comparatively 1975.The results of this research are reported little attention has been given to the behavior below. of any of the genus Pomacentrus Lacepede, since many species display persistent territoriality, Methods and materials thus lending themselves to easy observation. Field observations were made 3-5 times Low(1971)and Rasa(1969)studied teritorial- weekly in August 1973.In 1974,observations ity inP.flavicauda Whitley and P.jenkinsi began in early May and continued 2—,3 times

―151 ― 魚 類 学 雑 誌Japan.J.IchthyoL22(3),1975

weekly until July 1,except for a ten day period sponges,numerous soft coral,and occasional in June.From July 1 ti September 8,1•`3 sea anemones.Further south are smooth boul- study dives were made daily,except for August ders on sand.Outcroppings of table coral are 26 and August 30,when typhoons halted ob- scattered throughout the area. servations.From September 8•`October 31, Directly south of the cliff is a major breeding 2,3 dives were made per week.For the ground for Thalassoma cupido(Temminck and remainder of 1974,as in the winter of 1973, Schlegel)(Moyer,1974).The spawning and observations continued at 3•`4 dives per month. courtship of Stethojulis interrupta(Bleeker), The study continued throughout the 1975 Cirrhilabrus temminckii Bleeker(Moyer and breeding season. Shepard,1975),Labroides dimidiatus(Valen- SCUBA was used for all research.Various ciennes),and Cheilio inermis(Forsskal)have members of the TMBS staff aided in this study, also been observed.Pelagic eggs of these totalling more than 340 hours of underwater species,especially T.cupido,seem to account research.Depths and temperatures were read for a considerable percentage of the diet of from wrist guages.We tagged nests with P.nagasakiensis during the reproductive season. plastic markers numbered with grease pencils. Chromis isharai(Schmidt),C.flavomaculatus These were suspended from styrofoam floats Kamohara,and C.sp.from breeding colonies and secured with lead fishing weights.Indi- at the cliffs nearby,and Pomacentrus coelestis vidual fish were not marked,but could usually from the boulders south of the cliffs,gather be recognized by physical deformities,geo- with P.nagasakiensis in large feeding aggregates graphical location,and individual behavior, above the spawning wrasses daily during the which varied considerably within the popula- wrasse spawning season. tion.In 1975,plastic pipes,18 and 25 cm in Six Labroides dimidatus cleaning stations are diameter,were placed in the study area as nesting scattered throughout the study site.These are surfaces.These were subsequently used in supplemented by juvenile L.dimidiatus at fecundity studies. numerous places throughout the site in late Specimens collected for taxonomic identifica- summer and autumn.The abundance of tion are preserved in the Tanaka Memorial cleaners may have a direct effect on the desirabili- Biological Station under the following numbers ty of the area as a spawning site for so many TMBS 730726-08,TMBS 740716-02,TMBS pomacentrids and labrids. 741120-02,TMBS 741229-01(See Moyer and Results Ida,1975). In this paper,nests from 1973 and 1975 Pomacentrus nagasakiensis lives in loose ag- observations are numbered with the prefix 73 gregations.Our 1974 Igaya Bay study site or 75,e.g.73-01,75-01,etc.1974 nests are contained an aggregation of more than 30 P. identified merely by the nest number,e.g.1,3, nagasakiensis,of which at least 18 were males. etc. The actual nesting grounds covered an area of approximately 760 m2,and included a total of Description of study area 23 nests,of which no more than 18,more often Observations were made at various locations 16,were defended at any one time(Fig.1). around the island of Miyake; however,the Although the closest distance between successful major study site was in Igaya Bay on the west nests was only 2 m,usually at least 3e-4 m side of the island.The site covers an area of separated neighboring nests.Spawning com- approximately 2500 m2,ranging from 14•`16 m menced with the waxing of the moon in late in depth.A cliff,an ancient lava flow 2•`3 m in May in 1975 and early June in 1974,continuing height,is situated near the north end of the until late August in 1975 and early September study area.North of the cliff are loose in 1974.Differences between the years ap- volcanic rocks and boulders resting on sand. parently resulted from the earlier full moon The substrate south of the cliff consists of date in 1975.In both seasons,nesting con- large chunks of broken lava,rocks,and boul- tinued with at least one nest containing eggs at ders,covered with brown and red algae, all times throughout the season.Peak nesting

―152― Moyer:Reproductive Behavior of a Damselfish

interrupted reproduction and territorial activi- ties for a few days.Later,identical clusters appeared after a typhoon destroyed several nesting sites.In both of these examples,renewed nest construction,courtship,and spawning followed within a day or two.

Similar bunches of blue-headed individuals

observed on one occasion in the peak of breed-

ing activity in July,and again in late November,

long after the termination of the reproductive

season,confuse the picture.In both cases,

these were isolated observations and may have

been coincidental meetings of 3•`4 feeding

fish,or,in the July sighting,males attracted to

the same location away from their respective

Fig.1.Map of Pomacentrus nagasakiensis nesting territories by a passing female.In all cases,

population,1974.Numbers show locations blue foreheads would serve to inhibit aggression. of nests guarded by males.The shaded area Nest construction is the location of the feeding aggregate of Frequent observations suggest that nest con- non-territorial individuals.•¦=Labroides struction begins as soon as a suitable nesting dimidiatus cleaning stations. site is found.Usually nests are on the lower usually preceded each full moon by 2•`3 days surface of boulders.Construction involves throughout the breeding season. removing algae and invertebrates from the Clustering behavior nesting surface,and digging out sand,small The first suggestions of P.nagasakiensis shells,and stones.Only the male takes part activity begins in early May when water tem- in construction.Small stones and algae are peratures reach 20•Ž.During winter,only carried away and dropped,and clouds of sand scattered individuals can be seen in 16-19•Ž are blown out backwards by a rapid sculling of waters,and none have been observed when the caudal fin.Construction of a nest may temperatures drop below 15•Ž.Reproductive take from several hours to more than half a behavior begins as the water temperature reaches day,interrupted by lengthy journeys into the 22•Ž,with "clustering behavior"(See Keenley- water column to feed on plankton.Sometimes side,1972).Some males move away from their nests are abandoned before being used.In nesting sites of the previous year and begin 1974,Nest No.7 was abandoned and two others searching for new sites.Frequently,clusters of constructed in a period of two days.None 3•`6 fish can be observed in tight groups,facing was used. each other with deep blue foreheads.Blue Not infrequently,discarded junk is used as a foreheads normally signal appeasement in this nest site.Nest 73•`04 was constructed inside species,and are frequently flashed by intruding a rubber tire(Fig.2).Nest 73-12 was in an males when confronted by territorial males. old rice pot,and nest No.5,1974,was in a As none of the early season nest-hunting fish broken piece of plastic pipe. have yet established territories,this appease- Courtship ment signalling is not surprising,but the mean- a.Signal Jump ing of tight clusters of blue-headed fish is yet to Immediately after completion of nest con- be fully understood.That it is related to the struction,courtship begins in the form of signal establishment of territory is suggested by the jumps("Signalsprung",Abel,1961)by the male. frequency and timing of our observations.In P.nagasakiensis is primarily a plankton feeder, addition to numerous spring records,several and,except when guarding a nest,spends most similar clusters of blue-headed individuals were of the day feeding in loose aggregations 3•`5 m seen on August 20•`21,1974,when waters up in the water column.These aggregations warmed again after temperatures below 22•Ž tend to center at certain locations within the

―153― 魚 類 学 雑 誌Japan.J.Ichthyol.22(3),1975

Fig.2.Pamacentrus nagasakiensis Nest No.73-04,in a discarded tire.

borders of the breeding ground.When visi- phase begins to appear.Enticement colors

bility is good,it is possible to see the entire remain faint during signal jumps,but become

breeding ground from 5 m above the substrate. vivid and obvious when actual enticement

Therefore,signal jumps from nearby nest sites begins.An excellent photograph of P.naga-

are easily visible from feeding positions in the sakiensis in the enticement color phase was water column.Signal jumps begin as the fish published by Honda and'mai(1973).

swims slowly straight upward,propelled only by h.Enticement

simultaneous stokes of the pectoral fins,to a Enticement is an entirely different action

point perhaps 4 m above the substrate.The pattern from the signal jump,although entice- caudal fin remains motionless.Suddenly,he ment colors sometimes begin to appear in the

darts downward,usually in the direction of his signalling phase,and thus may be transitional

nest,with 3-4 fast sculling motions of the between the two action patterns.During entice-

caudal fin.The downward dash takes him ment,three blotchy grey bands appear on the

about 11/2•`2 m below the apex of the body; one extending from the top of the head

display.He then drifts up and repeats the over the eye to a point directly behind the eye,

pattern.Most frequently,signal jumps are per- another from about the third dorsal spine to formed in the immediate vicinity of the nest,but the lateral line or slightly lower,and the third

occasionally the nesting male may go quite directly anterior to the caudal peduncle.These

some distance to attract a female with the vary from dark grey in signal jumps to almost

looping display.The male from nest No.14 white in intense enticements.

was observed signal jumping 20 m from his The enticement display begins with the male

nest,near the feeding aggregation. rushing toward the approaching female in the

Signal jumps are often performed at random, blotchy color phase,quivering and swimming with no specific female in the immediate vicinity. with exaggerated motions of the caudal and

At such times,the signalling fish remains in the pectoral fins.As he approaches a point 10•` normal color phase.However,if a female moves 15 cm from her,he abruptly turns and dashes into visual range,the signalling action pattern back toward his nest,returning again and increases in speed,and the enticement color again,always in the same rapid exaggerated,

―154― Moyer:Reproductive Behavior of a Damselfish

quivering swimming motion and blotchy color. In this way he attempts to lead the female to his nest.Enticement motions are always orient- ed on a direct line between the female and the nest.The rapid caudal and pectoral beat continue throughout,while both approaching and leaving the female. Fig.3.Nesting success of Pomacentrus naga- Enticement only rarely results in spawning. sakiensis in relation to stages of the mean Not infrequently the female follows the enticing in July,August,and early September, male to his nest,but she rarely spawns.On 1974.N=new moon,F =full moon . one occasion,a female was followed for more than 15 min.She ranged freely over almost attention in this manner.As she approaches, the entire breeding colony.She entered five the signal jumps cease,and enticement displays nests,attracted by enticement displays,but begin.If these fail and the female moves on, did not spawn.Males enticed her out of other aggressive chasing and,rarely,biting follow.In male's nest sites,but no agonistic postures nor the rare cases when such attacks attract the chases were observed.Males moved far from interest of the female,enticement begins again. their nests(8,-10 m)to entice the female. Chasing of this nature is usually,but not always, They showed a variety of intensities of the performed by males in the enticement color blotchy enticement color phase.Some turned phase. it off as soon as she entered their nests,returning Chasing of females by males as a stage of to their normal color phase,but others,e .g. courtship is normally an action that follows No.13,remained blotchy throughout.It is unsuccessful attempts to entice the female into not uncommon to see 4•`5 males enticing a the nest.There are exceptions.No.8 not female at the same time,while another,a few infrequently left the signal jump phase to ag- meters away,performs signal jumps in faint gressively chase and sometimes bite the ap- enticement colors. proaching female.Interestingly,No.8 was by Pomacentrids are known to produce sounds far the most successful nesting male in 1974 in courtship(Allen,1972;Verway,1930).On (Fig.4). numerous occasions,P.nagasakiensis males d.Spawning were heard producing grunting sounds while Spawning commences with the male leading enticing females. the female into the nest with the enticement Rarely,the male on territory may show some display.The female touches the surface of the agonism toward an invading male.On one nesting rock with her lips,turns over and begins occasion(July 23,1974),No.10 was enticing a rubbing her abdomen over the surface of the female when No.8 interrupted and attempted rock with rapid beats of her pectoral fins and a to attract the female toward his nest.No.10 shuddering of the body.Her ovipositor pro- touched him on the side with his mouth and trudes about 2 mm.Creamy eggs are deposited extended all of his fins,but did not chase or bite. densely in a gradually widening patch over the Eventually No.8 enticed the female away from rock surface.The male follows behind,no his rival.Actual aggressive chasing of a male longer in blotchy enticement colors,occasionally by another male was observed only rarely.For touching the eggs with his lips,then turning over, example,No.12 attempted to entice a female his abdomen and protruding genital papilla ap- away from No.8,and was aggressively chased. pearing to rub over the freshly deposited eggs. Normally,little,if any agonism seems to be This is the "skimming" of Myrberg,et al.,1967. displayed between males during mutual court- His body quivers constantly as he propels himself ship of a female. with his pectoral fins in circles over the eggs. c.Chasing Not infrequently,either or both fish may leave Typically,signal jumps begin courtship dis- the nest for 2•`3 sec,immediately withdrawing plays.As soon as a female comes into sight, their genital papillae.Sometimes the male most males in the vicinity attempt to attract her leaves the nest to go into quivering enticement

―155― 魚 類 学 雑 誌JapanJ.Ichthyol.22(3),1975

Fig.4.Graph showing nesting success of individual Pomacentrus nagasakiensis males,Jul.15-Sep.7,1974 Bars indicate periods when nest contained eggs.Dotted bars indicates no observation possible due

to typhoon seas.•~=nest destroyed or abandoned.The dotted line at 22•Ž indicates the appar- ent minimum temperature of reproductive activity.N=new moon,F=full moon.

display with blotchy colors,returning seconds Spawning and courtship were most frequently later in normal colors to deposit more sperm, observed before 8:30 AM and after 3:00 PM after first touching the eggs with his lips.Both Mid-morning reproductive activity was regular, male and female occasionally stop spawning to but infrequent,apparently limited by almost fan the eggs daily morning feeding on the gametes of spawning At the. conclusion of spawning,the female Thalassoma cupido in the center of the P nagasa- leaves the nest,with the male often attempting to kiensis colony lead her back with a rapid enticement display Care .of eggs After a moment,he may touch her abdomen . with his lips,seem to lose interest and return to the Only the male tends the nest Females move nest to fan the eggs from male to male,with no attachment to any Eggs are laid . in densely compact clusters,our nesting territory,and males continue to entice samples varying from 160•~95mm to 230•~ passing females while tending eggs 190mm in size.Eggs are oblong in shape, Males with eggs rarely leave . the vicinity of the 0.5mm•~1.25mm.They are creamy in color nest,although short trips away from the eggs are when first deposited,changing to white,grey, rather common.These journeys vary from a few and finally silvery-grey before hatching seconds to 6•`8 min,and are usually to the Males continue to entice females,even. after water column nearby to feed on plankton or eggs are in the nest,and spawning usually occurs wrasse eggs,or to a Labroides dimidiatus clean- while eggs are already being tended.Nest No ing station.Activity at the nest consists of 8 often contained three separate clutches of eggs cleaning out debris and fanning the eggs.Oc- simulataneously.Usually the No.8 male was casionally,the male touches the eggs with his able to entice another female into his nest to lips.This action is apparently analogous to the "mouthing"of eggs in Amphiprion,described by spawn almost as soon as hatching eggs made space available,and therefore,he almost con- Allen(1972)and others In such cases,dead tinually tended eggs(Fig.4).Similar polyg- eggs are removed amous behavior occurs in P coelestis(personal Fanning . postures have been described by observation). Honda and Imai(1973)and will not be repeated

―156― Moyer:Reproductive Behavior of a Damselfish

here. Fecundity and male nesting success Nests are guarded from potential enemies. Pomacentrus nagasakiensis is a multiple Most frequently the pursued fish is Thalassoma spawner.Spawning occurs at any time between cupido.In addition,the following species have June and September,reaching peaks as the moon been observed being chased or attacked:Thalas- waxes.Eggs are small,egg patches are large,and soma lutescens(Lay and Bennett),Pteragogus the incubation period is short.Therefore,one flagellifera(Valenciennes),Cods sp.,Halichoeres would expect the fecundity of this species to be prosopeion(Bleeker),Choerodon azurio(Jordan rather high among pomacentrids.Since we did and Snyder),Stethojulis interrupta,Chromis not examine ovaries,we can only approximate isharai,Pomacentrus coelestis,Plotosus anguil- fecundity of females on the basis of male nesting laris(Lacepede),Pseudupeneus spilurus(Bleeker), success. Chaetodon nippon Steindachner and Doderlein, Pieces of plastic pipe,25 cm in diameter and Synodus variegata(Lacepede),and Gymnothorax 24 cm in length,were placed in the midst of the kidako(Temminck and Schlegel). breeding grounds.Eggs laid in these pipes were We have witnessed attacks on crabs,Percnon counted in the laboratory using a dissecting planissimus(Herbst) and shrimp,Palaemon microscope.Having thus determined the pacificus(Stimpson),in successful attempts to number of eggs per cm2,it was possible to make drive them from the nest. estimates of the number of eggs in a particular We were sometimes attacked while examining egg patch.The average nest patch computed in eggs.Usually the defender rushed directly at us this way contained about 21,000 eggs. to a point a few centimeters from our masks, Since observations were made almost daily, suddenly turning at right angles and stopping, it was possible to rather accurately estimate the with all fins extended.Some fish were more ag- number of egg patches guarded by each male gressive than others.Nos.73-01,73-03,and during the breeding season.There was con- No.2(1974)usually defended by backing into siderable variation in nesting success between the hand of the observer,with thrashing caudal males.In 1974,No.8 had eggs almost all the fins.Nos.73-02,and 5,8,and 18(1974) always made frontal attacks,biting the observers time,and since there was much overlapping of clutches,it was rather difficult to reach our hand or arm.Frequently clicking noises were estimate of 14 nest patches and about 294 heard just before the attack.Both Nos.5 and 8 ,000 eggs for his nest.Nos.6,11,12,and 14 were attacked their nest tags,and No.8 actually least successful of those fish regularly performing managed to carry his tag,with its comparatively signal jumps and enticements,with about five heavy lead weight,5 m from the nest. egg patches and 105,000 eggs for the year.Nos. Despite aggressive defense of eggs and nests, 1,2,3,4,5,10,and 13 had nests with eggs about many clutches of eggs are destroyed by predators. 10 times,amounting to approximately 210,000 We were never able to identify the responsible eggs each.From this we can estimate the fish or invertebrate,although T.cupido was once average number of eggs tended by a single male seen eating cases of hatched eggs.Nest No.16 to be somewhere between 200 was destroyed,the eggs eaten,and the male ap- ,000•`220,000 eggs in a season.Based on their studies of P. parently killed.Two morays,Gymnothorax nagasakiensis in Kyushu,Honda and Imai(1973) kidako,lay in the nest hole,and two shrimp, Palaemon pacificus,were on the rock surface estimate fecundity of this species at 211 ,000 eggs. where the eggs had been.The defender was never seen again.Shrimp usually move into Discussion empty nests,apparently to eat the egg cases,and a.Lunar periodicity and spawning may account for destruction of eggs from time to The influence of the moon on the reproductive time. behavior of marine animals is well known(Kor- Eggs hatch on the fourth or fifth night after ringa,1947).Among the pomacentrids,Allen spawning,varying apparently with water tem- (1972) has shown lunar periodicity for spawning peratures. of various species of Amphiprion at Eniwetok. That the spawning of P.nagasakiensis is influenc-

―157― 魚 類 学 雑 誌JapanJ.Ichthyo1.22(3),1975

ed by the moon is clearly shown in Fig.3.As the remained at 26-28•Ž for the next month. b.Clustering behavior moon waxes,spawning increases.At the July, 1974,new moon,only 6 nests had eggs.This Clustering behavior was first observed by Clarke(1971)among the garibaldi,Hypsypops number increased to 10 by the first quarter and reached a peak of 14 three days before the full rubicunda(Girard).He suggested that such behavior might represent a form of communal moon.After the full moon,there was a sudden decrease to a minimum of one nest with eggs courtship beginning prior to the regular breeding season.Keenleyside(1972)described similar two days before the new moon.In August, behavior in Abudefduf zonatus(Cuvier),and was nesting activity began to increase shortly after the first to use the term "clustering behavior". the new moon,reaching 9 nests with eggs by the He suggested that clustering might contribute to first quarter.Typhoon No.14 destroyed five breeding synchrony in local populations.Moyer nests shortly after,but new eggs in other nests and Sawyers(1973)observed clustering in brought the total up to 9 again two days before colonial nesting Amphiprion clarkii,again relat- the full moon. ing it to courtship behavior.Sale(personal com- In both months,peak activity preceded the full moon by 2•`3 days.Allen(1972)suggests munication)has observed such behavior in vari- ous Australian pomacentrids and identifies it that increased nesting as the full moon approach- es might improve conditions for nocturnal with the term"visiting behavior".In P.nagasa- kiensis,clustering occurs most frequently just egg care.Albrecht(1969)found increased egg care at night in two species of Chromis,adding prior to periods of intensive nesting,fitting well weight to Allen's point.Larvae of Amphiprion with the findings of Clarke(1971)and Keenley- and presumably other pomacentrids are posi- side(1972).Clustering appears to be a wide- tively phototactic,and,as Allen suggests,a spread behavior pattern in pomacentrids,and bright moon might stimulate freshly hatched further studies of its various forms and functions larvae to rise and join the plankton.Since are needed. c.Territoriality peak nesting comes 2•`3 days before the full moon in P.nagasakiensis,and since incubation is Studies of pomacentrid fishes have shown that only 3 1/2•`4 1/2 days,most eggs hatch within many are territorial only during periods of re- a few days of the full moon,providing maximum productive activity,e.g.Chromis chromis(Abel, light conditions for the hatchlings.However, 1961),C.multilineata(Myrberg,et al.,1967), much moonlight remains in the third quarter. C.ovalis(Steindachner)and C.verator Jordan Therefore,if phototaxis is a factor,preference of and Mets(Swerdloff,1970 a),C.isharai and C. P.nagasakiensis for the waxing moon suggests albomaculata Kamohara(personal observation), an early evening hatching hour.This possibility Dascyllus albisella Gill(Stevenson,1963), is supported by the fact that Honda and Imai Abudefduf abdominalis(Quoy and Gaimard)

(1973)found hatching to occur within an hour (Helfrich,1958),and A.saxatilis(Linnaeus) after sunset,and that the larvae were attracted (Fishelson,et al.,1974).Others,such as various to aquarium lights. species of Amphiprion(Allen,1972;Moyer and Cold water had a negative influence on Sawyers,1973),Hypsypops rubicunda(Limbaugh, spawning during the third quarter in August, 1964;Clarke,1970 and 1971),Abudefduf lacryma- when the water temperature plunged to 18.5•Ž tus(Quoy and Gaimard)and A.leucozona and stayed below 20•Ž for two days.During (Bleeker)(Fishelson,et at.,1974)persistently this period,many nests were abandoned,and defend territories. no signal jumps nor enticements were observed. Both types of territoriality are found in the The temperature reached 22•Ž by the new moon, genus Pomacentrus.Fishelson,et al.(1974) and nest construction and spawning began found P.albicaudatus and P.trichourus Giinther shortly after.A remarkable drop in nesting holding permanent territories,and Rasa(1969) activity had been noticed prior to the tempera- reports the same for P.jenkinsi.Low(1971) ture decrease.The sudden drop in reproductive reported P.flavicauda Whitley defending the activity after the September full moon was same territory over a period of five months,and clearly not related to water temperature,which Bardach(1958)suggested permanent territoriality

―158― Moyer:Reproductive Behavior of a Damselfish

for P.fuscus(Cuvier)and P.leucosticus.On the ing to take place.Secondly,the substrate must other hand,our studies of P.coelestis at Miyake be solid in order to provide absolute or near- show it defending territory only during periods absolute protection from the rear.Pipes, of active nesting. rice pots,tires,etc.,are ideal for this purpose,if Pomacentrus nagasakiensis seems to demon- large enough.In fact,if available,they are strate yet a third type of territoriality.Some invariably defended throughout the spawning individuals hold permanent territories and defend season,even if somewhat isolated from the rest them throughout the breeding season.Others of the aggregate,e.g.No.73-04.Brinley(1939) return to their nest sites and become territorial recorded a similar use of discarded junk in the only during periods of spawning,and a third form of cans,bottles,and even an old shovel,as type changes the location of his nest site and nesting sites of Eupomacentrus leucosticus Miil- territory one or more times during the repro- ler and Troschel,and Matsuoka(1962)was able ductive season. to get Pomacentrus coelestis to spawn in pieces of Allen(1972)points out that those species that pipe placed in the study site for that purpose.As defend territory only during reproductive activity for a natural nest site,boulders on a sand are primarily plankton feeders and,therefore,do substrate seem to be favored,since nests can be not need to permanently defend a limited area in constructed with comparative ease by fanning order to protect their food supply.This explana- out the sand. tion suffices for P.coelestis,a plankton feeder, Nests that seemed least desirable,e.g.7,9, but not for P.nagasakiensis.Although the 19,and 21,were located at relatively small latter almost exclusively feeds on plankton,many boulders that were either too upright to provide individuals are territorial throughout the breed- the limited shelter apparently required,or were ing season.Furthermore,those holding perma- too small and cramped to permit ideal spawning. nent territories seem to have the highest repro- A third factor seems to be related to shelter ductive success.For example,in 1974,males from surge during storms.This is especially true No.1,3,4,5,8,and 13 held permanent territo- where the substrate is sand.1974 nests Nos. ries and tended the most clutches of eggs.Nos. 2,7,10,11,19,and 20 were all in a long,shallow 2,10,11,and 12 returned to their territories only depression,where surge was strong.None was to spawn and had somewhat less successful defended persistently.All were destroyed by reproductive records.Nomadic individuals, drifting sand during Typhoon No.14,and the such as the male that occupied both nest Nos. male from No.2,easily identified by his split 9 and 21 and that at Nos.7 and 19.were the caudal fin,was never seen again.Robins(1957) least successful of all(Fig.4).An exception is noted that sand abrasion of the gill filaments and No.6,who defended his nest site from June to physical exhaustion are common causes of death September but had a very poor spawning record. during storms. Apparently,once a favorable nesting site is Obviously,the availability of females is an secured,it must be guarded continuously or important factor in the establishment of a perma- risk loss to another male.Males defending sites nent territory.A major mixed concentration of that for some reason may not be "suitable" feeding pomacentrids,including most of the defend them only at spawning peaks,spending female P.nagasakiensis in the population under most of their non-spawning time feeding on study,was observed almost daily in each year plankton,often far from their nests.Just near the top of the cliff,close to Nest No.5.A before spawning,they alternate between repairing weak current flowing seaward causes upwelling their previous nesting site and looking for a new along the cliff at that point,presumably resulting site.Territoriality,then,appears to be directly in concentrations of plankton in the compara- related to the"desirability"of the nesting site, tively narrow water column above the cliff. with the most suitable locations defended con- Signal jumps were performed in the vicinity of stantly. this group by Nos.1,5,6,and 14.Once at- Two obvious factors contribute to a suitable tracted to any of these males,signal jumps from nest site.One is the presence of a relatively the cluster of nests including Nos.3,4,7,and 19, smooth surface of sufficient size to permit spawn- could and often did lure females in their direc-

一459一 魚 類 学 雑 誌Japan.J.Ichthyol.22(3),1975

tion,where the signalling of other males became (Stevenson,1963).Species with concealed noticeable. nests or those protected by sea anemones would Labroides dimidiatus cleaning stations may also have the lowest fecundity.Pomacentrus naga- contribute in some way to the establishment of sakiensis eggs contrast with the dark rocks on

permanent territories.The successful cluster of which they are deposited,and little effort is made nests 3,4,8,12,and 18 were all within a few to conceal the nests.Therefore,eggs are rather meters of a cleaning station,as were Nos.1 and vulnerable to predation.Futhermore,like 14.Individuals from these nests were often Dascyllus and Chromis,Pomacentrus eggs hatch seen taking short trips to the wrasses.Cleaner early.This means that the larval fish are smaller, wrasses also bring females within enticement less efficient swimmers,and more subject to range of males nesting relatively far from the predation than the more developed Amphiprion feeding aggregate. species that hatch in relatively advanced stages The possibility that cleaning stations may after 6 1/2•`42 1/2 days(Allen,1972; Bell,in contribute to the nesting success of this species preparation). adds a new dimension to the studies of Slobodkin e.Sequential behavior patterns in reproduction and Fishelson(1974),which suggest that poma- Much attention has been given to analysis of centrids are relatively unaffected by the presence behavior patterns and their usefulness in tracing of Labroides dimidiatus. phylogenetic relationships in pomacentrids Since competition for food is not a factor in (Reese,1964; Myrberg,et al.,1967; Sale,1971; the territoriality of P.nagasakiensis,due to its Swerdloff,1970 a).Swerdloff(1970 a)proposed the following sequence of reproductive behavioral preference for plankton,active competition for nest sites seems to be the most important purpose phases : territorial delineation,preparation of for the establishment of territories.Competi- nest site,courtship,spawning and fertilization, tion for control over the most suitable sites is and parental care of eggs.Reese(1964)added 'severe,demanding persistent defense of such "selection of nest site"as a separate phase.In

territories once secured.In the population under P.nagasakiensis,selection of nest site and ter- study,sexually active males apparently out- ritorial delineation seem to be too closely related numbered ideal nesting sites,resulting in the to be distinguished as separate phases. different types of territoriality described. Within the courtship phase,the most well- d.Fecundity known of motor patterns in pomacentrids is Fecundity varies widely within the poma- the signal jump,first described by Abel(1961). centrids.Turner and Ebert(1962)estimated Swerdloff(1970 b)divides courtship into two 615,000 eggs for Chromis punctipinnis(Cooper) parts : the signal jump and skimming(see and Garnaud(1957)put Dascyllus trimaculatus Myrberg,et al.,1967).Albrecht(1969)added "chasing",which he considered closely related (Riippell)fecundity at 340,000•`425,000 eggs. Clarke(1970)found the average for Hypsypops to signal jumps,and Sale(1971)described a "high intensity signal jump".None of these rubicunda to be 129,000 eggs.At the other extreme,Allen(1972)estimated 3,000•`5,000 authors described enticement as a distinctive eggs per year for Amphiprion chrysopterus action pattern,although Sale's"high intensity Cuvier and 2,000•`4,000 eggs for A.perideraion signal jumps"have some similarities. Bleeker.Therefore,our estimate of Pomacentrus In Pomacentrus nagasakiensis,enticement nagasakiensis males guarding 200,000•`220,000 can be clearly recognized as a distinct behavioral eggs is about average fecundity among poma- pattern,easily distinguishable from signal jumps centrids so far studied. that usually precede it,and subsequent chasing Possible reasons for differences in fecundity and spawning that may or may not follow. are discussed by Swerdloff(1970).Highest Certain aspects of enticement may be transitional fecundity is found among fish with pelagic eggs. with signal jumps and spawning,e.g.the Nest-guarding pomacentrids have a much lower blotchy enticement color phase.However,the fecundity,as would be expected.Variation enticement action as a whole is distinct.An within the pomacentrids may be due to such almost identical enticement pattern occurs in factors as vulnerability of eggs,i.e.nest location P.coelestis,including blotchy enticement colors

―160― Moyer:Reproductive Behavior of a Damselfish

Fig.5.A typical nest of Pomacentrus nagasakiensis,showing white egg patch.(Nest No.1,1974)

(personal observation).We have observed similar enticements in Abudefduf sexfasciatus Acknowledgments (Lacepede) in the Bonin Islands,Chromis flavoma- Many students and staff members of the culatus,C.sp.,and Pomacentrus marginatus Tanaka Memorial Biological Station contributed Jenkins.Fishelson,et al.(1974)describe to this study.Particularly,I want to thank Rita pomacentrids"leading the females to spawn" Springsteen,Marco DiPaul,and John Shepard. after"signal swimming",but they do not Others to whom I owe special thanks are Bethy elaborate.We propose the following sequence Laun,Debbie Luekens,Kathy Meyer,Kazuyo of courtship behavior patterns for comparative Sato,and Bruce Tulloch.I am grateful to studies of pomacentrid fishes: signal jumps, Dr.Hitoshi Ida,Kitasato University;Dr. enticement,chasing,and skimming. M.H.A.Keenleyside,Western Ontario Univer- Not all of these patterns occur in all poma- sity;Dr.Peter Sale,University of Sydney;Dr. centrids.For example,we have never observed Yoshiaki Tominaga,Tokyo University;and Dr. signal jumps in Pomacentrus coelestis,presumably Teruya Uyeno,Nippon Luther Shingaku Univer- due to its small size and vulnerability to predation sity,who offered many helpful comments. if such an action pattern occured.Similarly, Mr.Torao Sato,Tokyo University,and Dr. Russell(1971)found no signal jumps in Chromis Ryoichi Arai,National Science Museum, dispilus Gunther.The limited home range of Tokyo,supplied important literature.Mr. various species of Amphiprion eliminate their Hajime Masuda,Tokai University,kindly need for signal jumps and enticements.The photographed Nest No.1 for use as Fig.5. lack of any of the proposed pre-spawning be- Finally,I especially want to thank Lori Bell,of havioral patterns in a particular pomacentrid TMBS,my constant diving and research com- can probably be explained with study.Such panion for two years,whose continuous enthusi- explanations would contribute to a better under - asm and encouragement inspired this study . standing of the evolutionary development of the family.

―161― 魚 類 学 雑 誌Japan.J.Ichthyol.22(3),1975

defduf zonatus (Pisces, Pomacentridae) at Heron

Literature cited Island, Great Barrier Reef. Animal Behavior , 20 (4) : 763•`774, Figs. 1•`4. Abel, E. F. 1961. Freiwasserstudien uber das For- tpflanzungsverhallen des monchfissches Chromis Korringa, P. 1947. The moon and periodicity in

Chromis Linne, einem vertueter der pomacentriden breeding of marine animals. Ecol. Monographs,

im mittlemeer.Z.Tierpsychol.,18(4):441•`449, 17 (3) : 349•`381, 5 figs. 7 figs. Limbaugh, C. 1964. Notes on the life history of

Albrecht,H.1969.Behavior of four species of two California pomacentrids : garibaldis, Hypsy- Atlantic damselfishes from Columbia,South pops rubicunda(Girard)and blacksmiths,Chromis

America,(Abudefduf saxatilis, A. taurus, Chromis punctipinnis (Cooper). Pac. Sci., 18 (1) : 41•`50,

multilineata,C.cyanea; Pisces Pomacentridae). 9 figs. Z.Tierpsychol.,26:662•`686,5 figs. Low,R.M.1971.Interspecific territoriality in a

Allen,G.R.1972.The anemonefishes:their clas- pomacentrid reef fish, Pomacentrus flavicauda

sification and biology.TFH Publications,Inc., Whitley. Ecology, 52 : 648•`654,2 figs. Neptune City, N. J., 1•`288, 140 figs., 23 tbs. Matsuoka, T. 1962. On the spawning of Pomacent-

Bardach, J. E. 1958. On the movements of certain rus coelestis Jordan and Starks.The Aquiculture, Bermuda reef fishes. Ecology, 39(1) : 139•`146, 10(3) : 1•`6.In Japanese.

3 figs, 3 tbs. Matsuoka, T. 1972. The fishes found in the rocky Bell, L. J. 1975. Notes on the fecundity of the shore of Shirahama, Ryugu-jima,Shimoda, and

anemonefish,Amphiprion clarkii, in Japan. In adjacent waters. Bull. Shizuoka Pref. Fish. Exp.

preparation. Station, 5 : 89•`111. In Japanese. Breder, C. M. Jr. and C. W. Coates. 1933. Repro- Moyer, J. T. 1974. Notes on the reproductive

duction and eggs of Pomacentrus leucoris Gilbert. behavior of the wrasse, Thalassoma cupido.

Amer.Mus.Novitates,612:1•`6,2 figs. Japan.J.Ichthyol.,21(1):34•`36. Breder, C. M. Jr. and D. E. Rosen. 1966. Modes Moyer, J. T. and H.Ida. 1975. Redescription of

of reproduction in fishes. American Mus.Nat. Pomacentrus nagasakiensis Tanaka and comparison

Hist., New York,941 pp. with specimens from Miyake-jima and the Bonin Brinley, F. J. 1939. Spawning habits and develop- Islands. Japan. J. Ichthyol., 22 (2) : 104—108,

ment of beau-gregory(Pomacentrus leucostictus). figs.1•`2.

Copeia, 4 : 185 188,1 fig. Moyer, J. T. and C. E. Sawyers.1973.Territorial behavior of the anemonefish, Amphiprion xanthurus, Clarke, T. A. 1970. Territorial behavior and popu- lation dynamics of a pomacentrid fish, the garibaldi, with notes on the life history. Japan. J.

Hypsypops rubicunda. Ecolog. Monogr., 40 : 189•` Ichthyol., 20 (2) : 85•`93, 2 figs. 212,11 figs. Moyer,J.T.and J.W.Shepard.1975.Notes on

Clarke, T. A. 1971 . Territory boundaries, court- the spawning and reproductive behavior of the wrasse, Cirrhilabrus temminckii. Japan. J. ship,and social behavior in the garibaldi, Hypsyops rubicunda(Pomacentridae).Copeia, 1971(2) : Ichthyol.,22(1):40•`42.

295•`299, 2 figs. Myrberg,A.A.Jr.,B.D.Brahy,and A.R.Emery. Fishelson,L., D.Popper and A. Avidor, 1974. 1967.Field observations on the reproduction of

Biosociology and ecology of pomacentrid fishes the damselfish,Chromis multilineata(Pomacentri-

around the Sinai Peninsula (northern Red Sea). dae) with additional notes on general behavior. Copeia,1967 (4) : 819•`827, 7 figs. J.Fish.Biol.,(1974) 6:119 ti 133,1 fig., 4 pls. Rasa, O. A. E. 1969. Territoriality and the estab- Garnaud, J. 1957.Ethologie des Dascyllus tri- maculatus(Rupp.).Bull.,Inst.Oceanogr.,54:1•` lishment of dominance by means of visual cues in Pomacentrus jenkinsi(Pisces: Pomacentridae). Z. 10,3 figs. Tierpsychol.,26:825 845,14 figs. Helfrich, P. 1958.The early life history and reproductive behavior of the maomao,Abudefduf Reese, E. S. 1964. Ethology and marine zoology.

abdominalis(Quoy and Gaimard).Ph.d.Disser- Oceangr. Mar. Biol. Ann. Rev., 2 : 455•`488.

tation,Univ. of Hawaii,228 pp. Robins, C. R. 1957. Effects of storms on the Honda,S. and S.Imai.1973. Breeding and early shallow water fish fauna of southern Florida with

development of a pomacentrid, Pomacentrus naga- new records of fish from Florida.Bull.Mar. sakiensis Tanaka in the aquarium. Mem. Fac. Sci.Gulf Carib.,7:266•`275,1 fig.

Fish, Kagoshima Univ., 20 (1) : 95•`106,8 figs., Russell,B.C.1971.Underwater observations on

1 tb.In Japanese. the reproductive activity of the demoiselle Chromis

Keenleyside,M.H.A.1972.The behavior of Abu- dispilus (Pisces:Pomacentridae). Mar. Biol., 10:

―16― Moyer:Reproductive Behavior of a Damselfish

22•`29, 6 figs. in Batavia Bay. Treubia, 12 (3-4): 350•`366. Sale, P. F. 1971. The reproductive behavior of the (Tatsuo Tanaka Memorial Biological Station, Toga pomacentrid fish, Chromis caeruleus. Z. Tierpsy- Farm, Ako, Miyake-jima, Tokyo 100-12 Japan) chol., 29: 156•`164, 3 figs.

Slobodkin, L. B. and L. Fishelson, 1974. The effect ナ ガ サ キ ス ズ メ ダ イ の 産 卵 生 態 of the cleaner fish Labroides dimidiatus on the

point diversity of fishes on the reef front at Eilat. 」3ckT.Moyer Am. Nat., 108 (961): 369•`376, 2 figs., 1 tb. 三 宅 島 に お い て1973年 か ら1975年 に か け ナ ガ サ Stevenson, R. A. 1963. Life history and behavior キ ス ズ メ ダ イ の 産 卵 生 態 を潜 水 観 察 に よ り調 査 し た. of Dascyllus albisella Gill, a pomacentrid reef 産 卵 行 動 は 水 温 が22。Cに 達 す る5.月 に 始 ま り9月 上

fish. Ph.d. Dissertation, Univ. of Hawaii, 1•`221. 旬 ま で 続 き,そ の 頻 度 は 月 齢 と 関 連 が あ り満 月 の2,3 Swerdloff, S. N. 1970 a. The comparative biology 日 前 に 最 も 活 発 と な る.他 の ス ズ メ ダ イ 類 と 同 様 に 雄

of two Hawaiian species of the damselfish genus が 転 石,タ イ ヤ,パ イ プ 等 の 面 を 掃 除 し 産 卵 床 を 造 り Chromis (Pomacentridae). Ph.d.dissertation, 卵 塊 を保 護 す る 。 産 卵 は 通 常 早 朝 あ る い は 夕 方 に 行 な

Univ. Hawaii, 1•`192. わ れ る が 求 愛 ― 産 卵 の 際 の 雄 の 一 連 の 行 動 は(1)signal, Swerdloff, S. N. 1970 b. Behavioral observations (2)enticement,(3)chasing,(4)skimmingの4形 に 分 け

on Eniwetok damselfishes (Pomacentridae: Chro- られ そ れ ら は 泳 ぎ 方,方 向 性,体 色 等 で 明 瞭 に 区 別 さ mis) with special reference to the spawning of れ る.雌 は1回 の 産 卵 で 数 千 の 卵 を 産 み,雄 は 通 常1 Chromis caeruleus. Copeia, 1970 (2): 371•`374, 産 卵 床 の 中 に3っ の 発 生 段 階 の 異 な る 卵 塊 を保 護 し, 2 figs. 受 精 卵 は5日 目 の 夜 に 艀 化 し1繁 殖 期 に ほ ぼ こ の 過 程

Turner, C. E. and E. E. Ebert. 1962. The nesting を 雄 は10回 繰 り 返 す.縄 張 り性 は 産 卵 期 間 の み に 発

of Chromis punctipinnis (Cooper) and a descrip- 達 し,そ の 強 さ は 産 卵 床 の 好 適 性 と 関 連 し て お り,好 tion of their eggs and larvea. Calif. Fish and 適 な 場 所 ほ ど 強 固 に か つ 長 期 間 守 られ 艀 化 す る 個 体 数

Game, 48: 243•`248, 7 figs. も 多 い 。

Verway, J. 1930. Coral reef studies. I. The (100-12東 京 都 三 宅 島 阿 古 富 賀 農 園 田 中 達 男 記 念 symbiosis between damselfishes and sea anemones 生 物 実 験 所)、

―163―