Japanese Journal of 魚 類 学 雑 誌 Vol.28,No.41982 28巻4号1982年

Social Behaviour and Mating System of the Gobiid Amblyeleotris japonica

Yasunobu Yanagisawa (Received March 26,1981)

Abstract The behaviour,social interactions and mating system of the gobiid fish Amblyeleotris japonica,that utilize the burrows dug by the snapping shrimp Alpheus bellulus as a sheltering and nesting site,were investigated at two localities on the southern coast of Japan.The fish spent most of their time in the area near the entrance of the burrow in daytime.Movements were limited to an area of about three metres in radius from the entrance.Aggressive encounters occurred between adjacent individuals sometimes resulting in changes of occupation of burrows. Males were more active in pair formation,whereas females were rather passive.Paris were usually maintained for several days or more,but some of them broke up without spawning.All the males that successfully spawned were larger ones that were socially dominant,and they re- mained within the burrow for four to seven days after spawning to care for a clutch of eggs. Variation in social interactions and burrow-use was recognized between two study populations and was attributed to the differences in predation pressure and density of burrows.

A number of of are known history and pair formation of the shrimp to live in the burrows of alpheid shrimps in Alpheus bellulus are described.In this study, tropical and subtropical waters(Luther,1958; the behaviour,social interactions and mating Klausewitz,1960,1969,1974a,b;Palmer,1963; system of its partner fish Amblyeleotris japonica Karplus et al.,1972a,b;Magnus,1967;Harada, are investigated and analyzed. 1969;Yanagisawa,1976,1978;Polunin and Lubbock,1977;Lubbock and Polunin,1977; Materials and methods

Hoese and Steene,1978).It is widely admitted Study area.Field work was carried out at that the association is a mutually beneficial Rinkai Beach,Tanabe Bay(33•‹41'N,135•‹20'E), partnership(Magnus,1967).For the fish the the Kii Peninsula and at Murote Beach,Uchiumi burrows are indispensable as shelter and for Bay(33•‹00'N,132•‹30'E),Shikoku Island.Both nesting.For the shrimps the tactile alarm coasts are exposed to the Kuroshio Current and communication developed between them and their faunas are similar.Sea surface tempera- the fish serves to avoid predation.Shrimps tures at both coasts are between 25•Ž and 28•Ž that emerge from the burrow maintain antennal in summer and seldom fall below 12•Ž in winter. contact with a fish posted at the entrance.The At Rinkai Beach,the gobiid fish A.japonica is shrimp detects the quivering motion of the abundantly found on the sandy bottom that goby's caudal part during unusual situations and borders the rocky reefs.A 9 m•~9 m quadrat reacts by immediate withdrawal into the burrow. was set on the sandy bottom at 4 m depth for Recently,considerable information has been repeated observations.At Murote Beach,A.

accumulated on the behaviour of the partner japonica occurs in the relatively narrow area associated in one burrow and the com- lying between the sand floor and the submerged munication between them(Preston,1978; rocks extending from cliffs.A 15 m•~40 m

Karplus,1979;Karplus et al.,1979),but no quadrat,divided into 5 m•~5 m sub-quadrats, investigation has been carried out on the as- was set on the bottom at the depths from 5 m sociated lives of these animals from popula- to 8 m. tional and developmental aspects. Field observations and collections.At Murote In another paper(Yanagisawa,MS.),the life Beach,the positions of the opened entrances of *Studies on the Interspecific Relationship be- the burrows of the shrimp in the quadrat and tween Gobiid Fish and Snapping Shrimp.III. the approximate sizes of fish that occupied the

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entrances were recorded monthly on a map tional dives were made at other hours to observe during the period from September 1978.to the diel activity of the fish and the shrimp.

August 1980 in order to obtain information on Collections were made at the above two the seasonal fluctuations of the population,the beaches and at other several localities.The growth rate of individuals and the frequency of body size of the specimens was measured to paired fish.A detailed census was also made in estimate crude growth pattern and to determine a narrow zone within the quadrat(2.5 m•~40 m) the size correlation between males and females to find even smaller entrances which were apt using the same burrow. to be overlooked in the whole quadrat cen- sus. Results

In order to investigate the daily positions and Growth.The majority of the gobiid fish daily changes of the social state of the fish,some Amblyeleotris japonica were found inhabiting of them were tagged in and near the quadrat at burrows of the snapping shrimp Alpheus bellulus

Rinkai Beach and in and near a 5 m•~5 m sub- and the rest were seen living in those of another quadrat at a shallower corner of the quadrat at shrimp A.rapacida.In addition,other gobiid

Murote Beach.The fish,caught by underwater ,Tomiyamichthys oni,Vanderhorstia fishing with SCUBA,were immediately anes- mertensi,Mahidolia mystacina and Stonogobiops thetized with quinaldine and tagged with a sp.,were also associated with the shrimps. coloured thread and a small coloured bead on The numbers of the above fishes found on the dorsum.Body size was measured and sex the bottom usually decreased during the cold was checked by the shape of the anal papillae. season when water temperatures fell below

Soon after recovery,they were released at the 15•Ž.In this period,they were apt to stay entrance of their burrows.Most of the tagged within the burrows and rarely appeared on the fish were acting in an ordinary way by the next substrate.Gravid females of all these species day.The tag usually lasted for three weeks or appeared from late June to the middle of August more.Twenty-three individuals were tagged and small juveniles were found on the bottom during the period from 5 August to 19 August from late July to early October.

1978 at Rinkai Beach,and 37 individuals during Seasonal variation in size-frequency distribu- the period from 12 July to 6 August 1979 at tion of A.japonica observed in the fixed quadrat

Murote Beach.Daily censuses and observa- of 100 m2 at Murote Beach is shown in Fig.1. tions were carried out during the period from The number of fish recorded in one census does

5 August to 3 September 1978 at the former site not necessarily represent the number of the and from 12 July to 17 August 1979 at the latter. whole population there,since fish in closed

The degree of gonad maturation of females was burrows,which could not be counted in the roughly recorded by their swollen abdomens census,may be significant,especially during the only at Murote Beach. winter.However,the numbers recorded in the

The behaviours of fish and shrimps were warmer season may safely be taken as a good observed and recorded in typically densely indication of the numbers of the whole popula- populated areas within and outside the quadrat tion.Sizes of all the specimens collected are at each beach.Fish are alert and ready to shown in Fig.2.From these two sources,the withdraw into the burrows when an observer crude growth pattern of the fish can be estimated approaches,but become habituated after re- as follows.The smallest juvenile collected was peated visits.By keeping motionless,their 8.7 mm in standard length and had transparent normal behaviour could be observed from close body with black pigments along the median line proximity.Although no perceivable sexual of the belly and five clumps of black pigments at dimorphism exists in this species,the sex of fish the positions where transverse bands of reddish in pairs could be determined in the field from brown will appear in the future.This juvenile, the difference in their body sizes and/or the which had presumably settled on the bottom swollen abdomen of the female. only a few days before,was already in associa-

These censuses and observations were usually tion with a similarly small shrimp in the burrow, carried out between 0900 and 1600,and addi- and was engaged in tactile alarm communica-

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Fig.1.Monthly size-frequency histogram of Amblyeleotris japonica in a 2.5 m•~40 m quadrat at Murote Beach.

Fig.2.Sizes of specimens of Amblyeleotris japonica collected during the period from 1972 to 1979. tion with it.Fish grew up to 20 mm to 40 mm fully developed gonads were found among those by the first winter,and most of them exceeded of more than 60 mm for females and 65 mm for a size of 50 mm by summer.Individuals with males.It is presumed from the monthly size-

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frequency histogram(Fig.1)that the number nearest neighbouring ones were 137 cm and

of settled fish decreased by about 80 % in one 65 cm,with standard deviations of 37 cm and year,both in 1978 and 1979.The adult popu- 19 cm,respectively. lation must be composed of individuals one The associations of juveniles soon after settle- and two years old,and those more than two years ment were composed of one fish and one shrimp

old are,if any,very rare(Fig.1). and those of young included one fish and one or

I have found no egg mass in the field,but in two shrimps.In the adult associations,the

the laboratory a pair of fish(female 77 mm and shrimps mostly occurred in pairs,whereas the

male 82 mm in standard length)laid eggs on the fish established pairs only in the warmer season. underside of an evaporation dish placed in an Pairs of fish appeared first in early May at both

aquarium in July 1973.The egg mass was bunch- beaches,about one and a half months before the

like,such as that of the gobiid fish Sicydium time when gravid females appeared.The ratio japonicum(Dotu and Mito,1955)and contained of associations in which two fish were witnessed

about 20,000 eggs.Eggs are ellipsoid in shape to the total associations at Rinkai Beach was

and 1.1 mm in length.Newly hatched larvae 7.6 % in July,7.3 % in August and 3.6% in

are 1.5 mm in total length. September.At Murote Beach,fish in pairs

Activity and use of burrows.As has been occurred during the same season as at Rinkai

described in another paper(Yanagisawa,MS.), Beach and the ratio to the total popula-

the gobiid fish A.japonica and its host snapping tion was nearly equal to that at Rinkai Beach

shrimps stay within the burrows during the in each month(Table 1).This is in con-

night,the entrances of which are closed with trast to the cases of other species,e.g.,T.oni

sediments.Soon after dawn,they start to ap- and Stonogobiops sp.,that paired in high fre-

pear on the bottom,the gobiid fish first break- quency throughout the year except the months ing through the sediment.Each burrow usu- from January to March when only few fishes

ally has one entrance opened at a time,the appeared on the substrate(Table 1).Pairs of position of which changes from day to day. A.japonica were always composed of hetero-

The number of entrances opened fluctuated sexuals and males were usually larger than

daily(Fig.3).The maximum density of the females by 5•`10 mm in standard length(Fig.

entrances was 0.31/m2 on 5 August 1978 at 4).

Rinkai Beach and 0.84 on 5 August 1979 at It was found from closer observations that

Murote Beach.On those days,the average some fish utilized two or more adjacent burrows

distances from one burrow entrance to the at a time,each of which accommodated a pair

Fig.3.Number of opened burrow entrances in a 9 m•~9 m quadrat at Rinkai Beach and in a 5 m•~5 m

quadrate at Murote Beach.

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Table 1.The proportion of individuals in pairs to the whole population in gobiid fishes as-

sociated with snapping shrimps in a 15 m•~40 m quadrat at Murote Beach.

Individuals less than 30 mm in standard length are omitted for A.japonica and T.oni and those less than

20 mm are omitted for V.mertensi and Stonogobiops sp. P,the number of paired individuals;W,the number of the whole population;F, P/W•~100(%).

Fig.4.Relationship between sizes of female and male in a pair. of shrimp.Such data have never been reported. shrimp.In solitary fish, individuals that Such fish travelled at indefinite intervals be- utilized more than one burrow were witnessed tween or among those burrows and stayed there only at Murote Beach.Paired fish not rarely to take up tactile communication with the used more than one burrow at a time at Murote

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Beach.Of 33 pairs observed for 20 to 40 within a radius of 3 m from the entrance.In minutes per pair,9 pairs used one burrow,21 an experiment in which fish caught by underwater pairs two burrows and 3 pairs three burrows. fishing were released at different sites on the At Rinkai Beach,on the contrary,of 19 pairs substrate,1,2,3 and 4 m apart from their observed for 30 minutes per pair,18 pairs used burrow entrances,those released at the point one burrow and 1 pair two burrows. four metres apart were never able to return Three places can be distinguished as having directly to their burrows in four observations, different meanings in the life of the gobiid fish: while those released at the points 1 to 3 m from the inside of the burrow,the entrance of the their burrow entrances often managed to return burrow and the substrate.The inside of the to their burrows within a few minutes.In burrow is used as a shelter and nesting place. another experiment in which fish were expelled The entrance and its vicinity are the area from from their burrows and chased persistently by which fish can safely retreat into the burrow an observer,they fled within a few metres radius when attacked.Their feeding behaviour was of the entrances of their burrows and after short mainly seen here.The duration of their stay time took refuge in their burrows or rarely in here has direct significance for the activity of the adjacent burrows.Even if the entrances had shrimps outside the burrow,since the shrimps been broken down beforehand by the observer, can emerge from the burrow only while they the expelled fish succeeded in returning to the can keep a tactile contact with the fish.The right points of their burrows.These observa- substrate apart from the entrance is the place tions suggest that fish know and recognize well where fish socially interact with neighbouring the bottom topography within some 3 m radius conspecifics.The relative duration of time of their burrows. fish spent in each place was compared.At Food and predators.The fish chiefly fed on Rinkai Beach,fish spent most of their time in benthic organisms on the substrate near the the area near the entrance.Paired fish spent entrances.Examination of stomach and in- 11.9 % of their time within the burrow,77.4 testinal contents revealed that more than 90 in the area near the entrance and% 10.7 % on of their food items were corophiid amphipods% the substrate apart from the entrance.Obser- and other small-sized crustacean species,as vations totalled 570 minutes for 19 individ- already reported by Harada(1969).These ani- uals.No quantitative observations were made mals are abundantly distributed over the sea for solitary fish,but they seemed to spend floor in areas where the burrows are dug and their time in the area near the entrance longer are in easy access by the fish outside their than paired ones.At Murote Beach,fish left burrows.Occasionally,all fish in a small area their burrows rather frequently.Solitary fish were observed feeding on planktonic organisms. spent 2.0,75.8 and 22.2 % of their time in In such cases,the fish dashed 1 to 5 cm above respective places during observations of 610 the sea floor,performing repeated biting motions. minutes for 28 individuals.Those values for This behaviour was usually observed near their paired fish were 2.5,63.6 and 33.9 % respectively burrow entrances.Young fish exhibited this in observations of 950 minutes for 40 bur- feeding behaviour more frequently than adult rows. and sub-adult fish(Table 2).The frequency of Fish rarely left their burrows for long dura- feeding motions of adult females was significant- tion.Rather,they repeatedly returned to the ly greater than that of adult males(Table 2). entrances of their burrows.The associated Although I have never seen living individuals shrimps often appeared from the inside of the of A.japonica being attacked and eaten by any burrows as soon as they returned,as if the animals under natural conditions,several times shrimps had been prepared to do so.The re- at Rinkai Beach I experienced that a gobiid fish peated returns of the fish clearly serve to facilitate was gulped by the lizardfish Trachinocephalus the activity of shrimps outside the burrows,and myops or the scorpion fish Sebastiscus mar- consequently may prevent the entrance from moratus the very moment I hooked it on my being blocked with sediment. underwater fishing line.The fish that escaped When leaving the burrows,fish usually ranged fter being hooked were also,attacked bya such

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Table 2.The frequency of feeding action of Amblyeleotris japonica per 10 minutes.

1,average;2,range predators.The gobiid fish never emerged from or head-to-head orientation(Fig.5d).This their burrows while predatory benthic fishes, display continues for several seconds or more, such as the stone fish.Inimicus japonicus and the and occasionally leads to circling.In"circling", above two species,were in the vicinity of their the two aggressive individuals intermittently burrows.They were also alert against car- circle each other,head-to-tail,each trying to nivorous fishes patrolling above the bottom, attack the caudal part of the opponent with its such as Therapon jarbua.On one occasion mouth.During fighting,bands on their bodies when one T.jarbua approached gobiids,it was fade away.This behaviour lasts for a long witnessed that the gobiids in a certain area time,up to 30 minutes.A scene of biting has simultaneously withdrew and took the posture not been observed,but there is no doubt that it of the posterior half of their body inserted into actually occurs,since the individuals whose the burrow or retreated wholly within the caudal fin or dorsal fins were partially torn off burrow.These potential predators were re- were not rare.Such individuals were mostly latively common at Rinkai Beach,and rarer at males. Murote Beach.The gobiid fish was rather in- Fish staying near their burrows were aggres- different to the approach of non-predatory sive against conspecifics invading their proximity. fishes,such as Geres oyena and Parapercis The residents approached the invaders and ex- snyderi. hibited lateral display and/or chasing to drive Aggressive behaviour.The encounter between them away.Fish using more than one burrow individuals of this gobiid species on the bot- were aggressive to the individuals that intruded tom raised one sided or mutual aggressive into any of their burrows.Mutual lateral behaviour.Four distinct types of aggressive display and circling occurred between two fish behaviour were observed:chasing,lateral of similar body size,and the resident fish often display,mutual lateral display and circling. won in the fighting.Aggressive encounters "Chasing"is essentially the same as seen in were frequently observed between males and any species of fish.One fish rushes towards prolonged fighting and circling were executed another to drive it away(Fig.5b).In "lateral only by males,whereas such encounters between display",one fish approaches the other with the females were relatively rare(Table 3). unpaired fins fully expanded and held stiffly, Table 3.Intersexual and intrasexual aggres- lifts the head with the mouth and the gill- sive encounters in Amblyeleotris japonica. opening widely opened,and slowly undulates the body(Fig.5c).At the same time,the five transverse brown bands on the body almost fade away.Lateral display is frequently fol- lowed by chasing.In"mutual lateral display", two fish place themselves side by side,spreading their fins and opening their mouths in the same fashion as in lateral display,with head-to-tail X,individuals whose sex was not certain

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Fig.5.Behaviours of the fish Amblyeleotris ,japonica.a:a fish staying near the burrow entrance with a shrimp Alpheus belhdus;b:a fish preparing to chase another fish;c:a fish exhibiting lateral display to an approaching fish;d:two fish engaged in mutual lateral display;e:a dominant fish returning to its burrow after a fighting with the adjacent fish;1:a fish soaring in the water.

The dominance of the fish was seemingly on the substrate nearby or in turn invaded other determined by the body size.Of 90 encoun- burrows.The subordinate fish sometimes sur- ters observed, the apparently smaller individ- rendered their burrows to the approaching uals defeated the larger ones only in three dominant ones even without demonstrating any cases.The dominant fish often intruded into defensive behaviour.The dominance and in- other burrows and stayed there after they chased feriority of the fish was also discernible from away the residents, although the occupation was their movement after fighting.The dominant usually temporary.The expelled ones stayed fish returned to their burrows, often swimming

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5 to 10 cm above the bottom with their fins within the burrow during the night,since no expanded and their body swaying(Fig.5e), individuals remained on the substrate at night. whereas the subordinate ones crept on the Floaters were usually very quick to seize an substrate with their fins folded. opportunity to occupy vacant burrows.They Most of the social behaviours mentioned here settled even in the burrow whose resident fish were observed at Murote Beach,since the was absent only for a moment,although they encounters between the individuals were rela- were driven away sooner or later by the resident. tively frequent at Murote Beach while such A fish that was a floater on one day was some- encounters were very rare at Rinkai Beach.A times observed being a resident on another day. On the other hand,some resident fish became possible reason for this difference may be that floaters after they had been expelled from their potential predators were rare at the former site and relatively common at the latter. burrows by the dominant fish.A floater may Floaters.Some portion of the population of be a more or less temporal condition and may A.japonica do not occupy burrows and result from social interactions among con- wander about on the substrate.These fish, specifics. hereafter called "floaters",were apparently Pairing behaviour.The bond between two smaller than the residents of burrows(x2,P< paired fish was often loose,especially early in 0.01)(Table 4).They represented 2.1 % of the reproductive season.One fish of a loose the total population at Rinkai Beach and 5.3 pair often visited the adjacent burrow which was at Murote Beach in summer.The floaters occupied by the other and returned to its original remained usually within a relatively small range burrow after a short stay there.In such a case, on the substrate and showed a tendency to it was occasionally observed that the resident, stay at the site nearly equidistant from the when it was a female,nudged the belly of the adjacent residents,since they received attacks visitor with the snout while the latter was from the residents if they approached nearer staying near the entrance of the burrow.Soon the entrances of burrows.Forty-five % of ag- after the visitor received the action,it always gressive behaviour of the residents were directed departed.This action may be a signal by at floaters. which a resident mildly refuses to form a pair. Males were more active in pair formation, When driven off by an observer,a floater moved about on the floor or took refuge into and severe fightings were observed between one of nearby burrows of shrimps.In the latter males.Of four cases of circling observed at case,it always entered the burrow after the Murote Beach,three were obviously concerned resident fish of the burrow did first,and then it with the acquisition of a mate by two males. reemerged from the burrow before the resident The most outstanding fighting was observed on did.In 14 cases in which the observer ap- 30 July 1979 between the tagged male M4 and an untagged male X of similar body size. proached a floater and let it retreat into a burrow,the floater stayed within the burrow Until that day,the male M4 had paired with the only for an average of 52 seconds per one retreat, female F2 for 10 days and they had occupied while the resident remained for 91 seconds.It two adjacent burrows,and the male X had appeared that each floater had a definite burrow utilized a burrow 1 m apart from those of the into which it temporarily sheltered itself when pair.The two males were found engaged in exposed to danger,and it probably lodges circling on the substrate near one of the burrows

Table 4.Size-frequency of residents of burrows and floaters in Amblyeleotris japonica at Murote Beach in summer.

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of M4,and the circling intermittently lasted for five times as long as males did.This means 30 minutes.While the males were fighting, that female fish provide facility more often for female F2 stayed on the sand floor or on a the activity of shrimps outside the burrow than small stone near the males and then moved to male fish do,since shrimps emerge from the the burrow of X.Male X stopped fighting burrow only while fish stay in the proximity of soon after the female went to its burrow,and it the entrance or the depression.Feeding be- went there,too.On the next day,X and F2 haviour of females occurred in higher frequency were observed paired and inhabiting the burrow than that of males.In experimental situations of X,whereas M4 was a floater and kept mo- of slow approach of a diver to a pair of fish tionless on the substrate near its original burrow staying at the entrance,intended to determine with its heavily broken dorsal fins folded.Its which mate was more sensitive to danger,males burrows were occupied by another male. retreated first into the burrow in most trials and Males occasionally performed one peculiar females reemerged first from the burrow without action,"soaring".Holding their bodies per- exception(Table 5).Males stayed within the pendicular to the bottom,they rose up 10 to burrow three times as long as females per each 40cm in the water,and remained motionless retreat. there for 5 to 30 seconds with the unpaired fins Change of occupied burrows.At Rinkai expanded(Fig.5f).Brown bands on the body Beach,twenty-four individuals were tagged in almost faded out just before and during this and near the 9m•~9m quadrat in August 1978, action.The pale body apparently reduced its which represented about a half of the whole conspicuousness in the water.It was exhibited population there.The daily records of the by males that were paired or going to form positions of the entrances of the burrows they pairs and mainly on the occasions when they occupied during the period from the day when were separated from their mates or were just they were tagged to 3 September 1978 are shown after aggressive encounters with rivals.After in Fig.6.The positional change of the burrow soaring,the males often moved to the burrows entrance of tagged fish between successive days of their mates or rivals.It is very probable was simply due to the change in the position of that by soaring the males reconnoitre the sur- the entrance of the burrow itself in 184 cases, roundings,especially the positions and behav- and only in 15 cases it was caused by the move- iour of their mates and rivals.I have never ment of the fish between different burrows.In seen females performing this action. the latter cases,the movements of the fish M4 In an established pair,no aggressive behaviour and F8 were done respectively between burrows was seen between the mates.A display similar 5 m and 10 m apart from each other,but other to mutual lateral display was frequently observed movements were between adjacent burrows. near the entrance of their burrow when either Five cases were obviously concerned with pair of them returned to the burrow after a prolonged formation.Fourteen tagged fish stayed in their absence.They approached each other and particular burrows throughout the observation erected their fins,opening their mouths,but this period. behaviour ceased after three seconds or so and At Murote Beach,37 individuals were tagged thereafter they remained close together.It may in and near the 5m •~5m quadrat in July and be regarded as a ritualized greeting display August 1979,representing about two thirds of rather than an aggressive behaviour. the whole population there.Changes in the Some behavioural differences were observed positions of their burrow entrances during the between male and female of a pair(Table 5). period from the day when they were tagged to Males stayed within the burrow longer than 17 August 1979 are shown in Fig.7.In the females.Males wandered on the substrate cases where one individual used more than one apart from the entrance for a considerably longer burrow within one census,the position of either time than females.In the burrow with a de- burrow was recorded as the position of the in- pression extending from the entrance on the dividual.The positions of the burrow entrances bottom surface which was formed by shrimps, where each fish was stationed were confined females stayed at the distal part of the depression within the area of about 5 to 10 m2.Since

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Table 5.Differential behaviours between female and male in a pair.

it was impossible to identify the entrance of a termined from short observations.At Murote certain burrow on one day with that on the Beach,the condition of,paired residents was other days and therefore impossible to estimate divided into two,that is,stably paired and the extent of one burrow,the number of bur- transiently paired,although the discrimination rows utilized by each fish during the study period between them is more or less arbitrary. could not be determined definitely.However, At Rinkai Beach,each fish did not appear on there is no doubt that most fish used more the substrate on many days,and therefore the than one burrow,probably from two to as complete sequence of the social condition of many as six burrows.For instance,it is esti- such individuals could not be obtained.About mated from the positional changes that the fish half of the tagged fish remained solitary through- M14 moved among four adjacent burrows and out the study period.Pairs were formed be- the fish M10 among six burrows (Fig.7).The tween larger individuals and maintained for ranges of the positions of the burrow entrances several days or so(Table 6). of particular tagged fish during the study period At Murote Beach,males smaller than 70 mm greatly overlapped one another,indicating that and females smaller than 65 mm in standard each burrow was occupied alternately by more length rarely paired(Table 7).Males that were than one fish. large enough but slender,such as MI and M11, It was ascertained in the fish M1 and F8, rarely paired.Pairs often terminated in a few whose tags fortunately endured for a long time, days,and the members of a pair sometimes that both had stayed in a few definite burrows changed.In a few cases,two fish that had once throughout four months. formed a pair paired again after a long period Change of social state.The social state of of separation.For instance,the male M5 and the fish was categorized into three conditions, the female F13 that were observed paired from i.e.,paired resident,solitary resident and float- 25 to 27 July,paired again on 17 August. er,and was observed daily for tagged fish at Some of pairs were maintained for a.long time. both beaches.The sequences of the social con- For instance,the male M6 and the ,female F5 ditions at successive days surveyed are shown were in a pair on many days during .the study for each tagged fish in Tables 6 and 7.Some period,and the pair of the male .M4 and the of the fish regarded as solitary may have been female F2 continued for 10 days.Some of the actually paired,since their social state was de- fish formed pairs with more than one fish during

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Fig.6.Daily changes in the position of tagged individuals at Rinkai Beach during the period from the day when they were tagged to 3 September 1978.Females and males are shown on separate maps Positions of each individual in two successive days are linked with a line.Each dotted area. re presents the horizontal extent of one burrow inferred from daily shifts in the position of burrow entrance.

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Fig.7.Daily changes in the position of tagged individuals at Murote Beach during the period from the day when they were tagged to 17 August 1979.Females and males are shown on separate maps. Positions of each individual in two successive days are linked with a line.Since the movement areas of individuals overlapped one another,the movements of nine individuals(F4,F10,F19, F20,F21,M10,M12,M13 and M15)are shown within dotted areas in the margin and their actual places in the map are represented by dotted areas.Areas A to F encircled by a line are the posi tions of burrows referred to in Fig.8.

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Fig.8.Occupation of burrows by one female F7 and two opponent males M10 and M14.Positionsof burrows are shown in Fig.7.For details see text. the study period.The male M13 paired with that day.Thereafter,they were solitary on two females at a time on 31 July and 1 August, the substrate at least for four days.On the although each pair was not stably established. other hand,the males that had paired with The social state of the tagged fish often them were never found on the substrate for changed as a result of social interactions with four to seven days after that presumed spawning adjacent fish,accompanying the movements of day.The absence of M6 from 23 to 28 July, the fish between burrows.The most remarkable M8 from 3 to 7 August and from 9 or 10 to 12 change of social state was exhibited by the male August,M14 from 7 to 10 August and M15 M10 that competed with M14 for the acquisi- from 9 or 10 to 14 August were such cases tion of F7(Fig.8).The male M10 remained (Table 7).This sort of absence was also seen paired with F7 and kept two burrows(burrows in M3 from 3 to 7 August after it had paired C and D in Fig.7)under their control on 24 with an untagged gravid female.Probably, and 25 July.However,M14,appearing from the males were staying within the burrows to somewhere,replaced M10 as a mate of F7 and care for and guard a clutch of eggs during that occupied the burrows A and B on 27 July. period.If so,the duration of incubation may After M14 and F7 established a stable partner- be estimated to be between four and seven days. ship,M10 was frequently attacked by M14 and The female probably did not guard the eggs, was forced to move from the burrow C to the since they were observed on the substrate after burrow D or E.It moved to burrow A and spawning. became dominant there for a few days while All males and females that were presumed to M14 disappeared on the substrate(7 to 10 have participated in spawning were the dominant August),but was driven away to burrow F after ones,and they were presumed to have spawned M14 reappeared. only once in the study period.The male M8 was Mating.The belly of every adult female was the exception and it spawned twice,once with more or less swollen throughout the reproductive F9 on 1 August and a second time with F8 on 8 season,but gravid females with remarkably August,and one additional spawning around on swollen bellies were found among the pairs. 24 July may have occurred,since it had stayed Of such gravid females at Murote Beach,F5 within the burrow from 24 to 29 July(Table 7). on 22 July,F2 on 31 July,F9 and F18 on 1 Discussion August,F7 on 6 August and F8 and F21 on 8 August displayed normal abdomens and be- Activity and mating.The number of fish came solitary on the following day(Table 7). species on the sandy bottom is usually much Each of them_.probably spawned on or around smaller.than that in the rocky or coral area.

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Those species that can burrow by themselves or staying here have the advantage not only of utilize burrows made by other animals may take safe shelter for themselves in the burrows when the sandy bottom as an advantageous habitat. attacked,but also to provide a facility to the The gobiid fish Amblyeleotris japonica cannot shrimps for sustaining the burrows.They need provide themselves with sheltering burrows,and not move great distances from burrow entrances unless there are burrows dug by snapping for food,since food items are generally plentiful shrimps,the sandy bottom is not an available on the sandy bottom and they can easily get habitat to them.For this species,to obtain enough food.However,they have to journey partner shrimps and to protect them from at- over the substrate to acquire their mate. tacks by predators are equivalent to the ac Fish did not move around freely over the quisition of living place and are requisite to its substrate.Fish wandering on the substrate life. were often attacked by the adjacent resident fish, As has been shown,the fish A.japonica and rarely ventured more than some 3 m spend more than 60% of the time in the area from their burrows.Changes in the occupation near the burrow entrance in daytime.Fish of burrows,if they occurred,were usually be-

Table 7.Daily observations on social condi tions

―416― Yanagisawa:Gobiid Behaviour tween adjacent ones.Some fish were observed in this species may be accounted for by the fact using a few definite burrows throughout several that only a small portion of females are gravid months.These results suggest that the fish is at one time while most adult males are seemingly rather stationary.This means that the number sexually active throughout the breeding season, of potential mates each fish can encounter is resulting in the fact that the ratio of fertilizable limited to a few,suggesting that the competition females to sexually active males in one area at for acquisition of mates is severe among neigh- any given time is biased towards males,like bouring consexuals. most species. As has been shown,the competition was Pairs of adult fish appeared one and a half much more severe among males than among months before the females became gravid,but females.Males were usually ready to form were often loose and broke up without spawn- pairs and prolonged fighting was observed be- ing.Paired males were sometimes attacked and tween males,whereas females were rather passive replaced by other males.All the males that and sometimes refused to form a pair.The were presumed to have successfully spawned competitiveness and contentiousness of males were the larger ones that were socially dominant.

of tagged individuals at Murote Beach.

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Table 7.

F,female;M,male;o,solitary;P,stably paired resident;T,transiently paired resident.Each fish was A figure below P or T means the individual number of its mate,x meaning that its mate is untagged.Female

However,most males spawned only once during pair bonding between the two animals may be the study period,suggesting that the degree of attributed in part to differences in the way of monopolization of spawning by one dominant obtaining a mate.A solitary fish can meet male is not extreme.This may be attributed with individuals of the opposite sex by moving to the breeding habit of this species where one on the substrate from one burrow to another, male breeds with only one female at a time and while a solitary shrimp in the isolated burrow thereafter it takes several days to care for the has a chance to encounter a mate only through clutch of eggs within the burrow. the connection of its burrow with the adjacent Although both this gobiid fish and its host burrow within the sediment(Yanagisawa,MS.). shrimp, Alpheus bellulus,take the burrows as The number of potential mates accessible to each their habitat,they have quite different patterns individual may be greater in the former animal of pair bonding.In the shrimp,some in- than the latter.Individual fish probably gain dividuals form pairs even at the juvenile stage little or no reproductive advantage by establish- and adult individuals usually occur in pairs. ing pair bonds at an early stage of life,long The pair bonds are usually stable and some of before maturation.Rather,to share one bur- them are maintained for several months(Yanagi- row with another fish for a long time may be sawa,MS.).The difference in the pattern of less advantageous to each fish than to have one

―418― Yanagisawa:Gobiid Behaviour

(continued)

tagged on the first day in the record.A blank column shows that the fish was not observed on the substrate. or mate of male with a swollen belly is indicated with a symbol(*).

burrow all to itself,since the space of the burrow the number of individuals that stay on the is not wide. substrate apart from their burrows.At some Nevertheless,the pair bond in this gobiid localities,the majority of fish attached them- fish,which is usually maintained for several selves to the entrances of burrows and were days or more,is exceptionally stable among the alert and ready to withdraw into the burrows. species of Gobiidae(Breder and Rosen,1966). At other localities,on the contrary,a number of In most of gobiid fishes,females and males live fish moved freely away from their burrows and together only while they are engaged in courtship returned to their burrows rather sluggishly when and spawning behaviours.Relatively stable a diver approached.This impression of differ- pair bonds in this species may be attributed to ence was also ascertained in the two populations the condition that its habitat is discontinuous in this study.Fish at Rinkai Beach spent most and potential mates that one individual can of their time in close proximity to the entrances encounter are not abundant owing to their and the total length of their stay on the substrate restricted home range. was shorter,as compared with those at Murote Variation in behaviour.I have an impression Beach. from observations on various coasts in Japan This variation seems to be related to the that there is great variability in this species in difference of predation pressure between the

―419― 魚類学雑誌 Japan.J.Ichthyol.28(4),1982

localities :potential predators are relatively ficult.In the two populations studied,no common at Rinkai Beach but rarer at Murote essential differences were perceived both in the Beach.It is quite reasonable that fish under timing of pair formation and the stability of the high predation pressure adhere to the burrow pair bond,as mentioned above.Presumably, entrances to lower the probability of attack. the difference in difficulty of movement between The density of burrows may be also responsible burrows is not critical enough to bring about an for this variation:the density of burrows at obvious variation in the pattern of pair bonding Murote Beach was about three times as high as between them.However,a somewhat different at Rinkai Beach.Even within the same locality, pattern was perceived in another population.At there was a tendency that fish in the densely Motogoe Beach near Murote Beach,out of 10 populated area left their burrows more fre- burrows which were isolated from one another quently than those in the sparsely populated by more than 4 m distance,three burrows were area.Fish in areas where burrows are closely occupied by established pairs of fish in the distributed may be able to shelter themselves middle of April when no pairs were found at more easily and safely in any of the burrows Murote Beach,suggesting that pairs are estab- when attacked by predators. lished earlier in sparsely distributed populations . Differences were also noticed in other be- As has been described,the gobiid fishes haviours and social interactions between the Tomiyamichthys oni and Stonogobiops sp.that two populations.At Rinkai Beach,each fish are sparsely populated at Murote Beach pre- usually used one burrow at a time and stayed in sented a remarkable difference in the pattern of one particular burrow over some weeks.At pair bonding from the fish A.japonica.Pairs in Murote Beach,one to two burrows were used those two species were found nearly all the year by one solitary fish and one to three burrows by round(Table 1)and some pairs were established one pair at a time,and each fish moved among by small individuals long before maturation. two to six burrows within a month.In the The difference of those species from A.japonica former population,aggressive encounters be- may be related to the difference of population tween individuals were much rater and the pro- density and therefore to the difference in the portion of floaters to the whole population was availability of mates,but cannot be attributed smaller than in the latter population.These only to these factors.In A.japonica,neither differences may also be explained by the above pairs in the winter nor those between small two ecological parameters,i.e.,predation pres- individuals long before maturation have been sure and the density of burrows.In areas found in any localities.The feature of pair where leaving a burrow is hazardous for a fish bonding may be to some extent a species- owing to the high predation pressure and the specific characteristic. low density of burrows,it may be profitable for Recently,the variation in behaviour and so- the fish to adhere to one definite burrow both in cial organization of various fish species has been short term and long term.Consequently,the related to the ecological parameters that are frequency of encounters among the individuals different from one locality to another(Keenley- will be kept low.Floaters will not be allowed side,1979;Fricke,1980:Moyer,1980).In the to survive for a long time due to high predation coral-dwelling damselfish Dascyllus marginatus, pressure. the variation in mating system is attributed to These two ecological parameters may also one ecological parameter:the number of availa- have an influence on the pattern of pair bonding. ble hiding places in the coral(Fricke,1980). As has been discussed in another paper(Yana- In the anemonefish Amphiprion clarkii,the gisawa,MS.),for the animals living in the dis- population in warm temperate waters shows crete habitat each unit of which is so small that many differences in behaviour and social interac- only a few individuals can be accommodated in tion when compared to populations in the it,the timing of pair formation and the stability tropics,and such differences are attributed to of the pair bond depend on the degree to which differences in water temperatures,predation a mate is hard to obtain and hence to which pressure and the size of host anemones(Moyer, movement between units of the habitat is dif- 1980).These fish live in a discrete habitat,each

―420― Yanagisawa:Gobiid Behaviour unit of which has only a small space,similar to gobiid fish in the northern Red Sea. Mar. Biol., the gobiid fish A.japonica.For fishes living in 24: 259•`268, figs. 1•`6. such habitats,the size of one unit of the habitat Karplus, I., M. Tsurnamal and R. Szlep. 1972b. Analysis of the mutual attraction in the association and the difficulty in movement between units of the fish Cryptocentrus cryptocentus (Gobiidae) must be critical factors in regulating the behav- and the shrimp Alpheus djiboutensis (). iour of individuals and determining the social Mar. Biol., 17: 275•`283, figs. 1•`9. organization.These ecological parameters may Karplus, I., M. Tsurnamal, R. Szlep and D. Algom. be changeable enough from place to place to 1979. Film analysis of the tactile communication bring about perceivable variation in behaviour between Cryptocentrus steinitzi (Pisces, Gobiidae) and social organization. and Alpheus purpurilenticularis (Crustacea, Al-

pheidae). Z. Tierpsychol., 49: 337•`351, figs. Acknowledgements 1•`6. Keenleyside, M. H. A. 1979. Diversity and adapta- I wish to express my sincere thanks to Prof. tion in fish behaviour. Springer-Verlag, Berlin, Eiji Harada for his invaluable advice and critical xiii+208 pp.67 figs.

reading of the manuscript.Prof.Tatsumi Klausewitz, W. 1960. Fische aus dem Roten Meer. Uematsu and Mr.Tetsuo Kuwamura have IV. Einige systematisch and okologisch bemer-

kindly informed me of literature,for which I kenswerte Meergrundeln (Pisces, Gobiidae). Senck. am indebted.I express my thanks to Prof. Biol., 41 (3/4): 149•`162, figs. 1•`10. Takeo Ito and Dr.Nobuhiko Mizuno for their Klausewitz, W. 1969. Fishe aus dem Roten Meer. helpful suggestions,and to Messrs.Yasuo Nii- XI. Cryptocentrus sungami n. sp. (Pisces, mura,Hideo Suga and Shigeyuki Yamato for Gobiidae). Senck. Biol., 50 (1/2): 41•`46, figs. their willing assistance in the field. 1•`4. Klausewitz, W. 1974a. Fische aus dem Roten Meer.

Literature cited XIII. Cryptocentrus steinitzi n. sp., ein neuer "Symbiose -Gobiide"(Pisces: Gobiidae). Senck.

Breder, C. M. and D. E. Rosen. 1966. Modes of Biol., 55 (1/3): 69•`76, figs. 1•`2.

reproduction in fishes. American Mus. Nat. Klausewitz, W. 1974b. Fische aus dem Roten Meer.

Hist., New York, 941 pp. XIV. Eilatia lantruncularia n. gen. n. sp. and Dotu, Y. and S. Mito. 1955. Life history of a n. sp. vom Golf von Aqaba

gobioid fish, Sicydium japonicum Tanaka. Sci. (Pisces: Gobiidae: ). Senck. Biol., 55 Bull. Fac. Agr., Kyushu Univ., 15 (2): 213 N 221, (4/6): 205•`212, figs. 1•`7. figs. 1•`4. (In Japanese). Lubbock, R. and N. V. C. Polunin. 1977. Notes on Fricke, H. W. 1980. Control of different mating the Indo-West Pacific Ctenogobiops (Tele- systems in a coral reef fish by one environmental ostei: Gobiinae), with descriptions of three new factor. Anim. Behay., 28 (2): 561•`569, figs. 1•`4. species. Revue Suisse Zool., 84: 505•`514, figs. Harada, E. 1969. On the interspecific association 1•`9. of a snapping shrimp and gobioid fishes. Publ. Luther, W. 1958. Symbiose von Fischen (Gobiidae) Seto Mar. Biol. Lab., 16 (5): 315•`334, figs. 1•`10. mit einem Krebs (Alpheus djiboutensis) im Roten Hoese, D. H. and R. Steene. 1978. Amblyeleotris Meer. Z. Tierpsychol., 15: 175- 177, figs. 1•`3. randalli, a new species of gobiid fish living in as- Magnus, D. B. E. 1967. Zur Okologie sediment- sociation with alphaeid shrimps. Rec. West. bewohnender Alpheus-Garnelen (Decapoda, Aust. Mus., 6 (4): 379•`389, figs. 1•`3. Natantia) des Roten Meeres. Hergolander Wiss. Karplus, I. 1979. The tactile communication be- Meeresunters., 15: 506•`522, figs. 1•`7. tween Cryptocentrus steinitzi (Pisces, Gobiidae) Moyer, J. T. 1980. Influence of temperate waters and Alpheus purpurilenticularis (Crustacea, Al- on the behavior of the tropical anemonefish pheidae). Z. Tierpsychol., 49: 173•`196, figs. Amphiprion clarkii at Miyake jima, Japan. Bull. 1•`13. Mar. Sci., 30: 261•`272, figs. 1•`2. Karplus, I., R. Szlep and M. Tsurnamal. 1972a. Palmer, G. 1963. A record of the gobiid fish Associative behavior of the fish Cryptocentrus cryptocentrus (Gobiidae) and the pistol shrimp Cryptocentrus lutheri Klausewitz from the Persian Gulf, with note on the genus Cryptocentrus. Alpheus djiboutensis (Alpheidae) in artificial bur- rows. Mar. Biol., 15: 95•`104, figs. 1•`13. Senck. Biol., 44 (6): 447•`450, 1 fig. Karplus, I., R. Szlep and M. Tsurnamal. 1974. Polunin, N. V. C. and R. Lubbock. 1977. Prawn- The burrows of alpheid shrimp associated with associated gobies (Teleostei: Gobiidae) from the

―421― 魚類学雑誌 Japan.J.Ichthyol.28(4),1982

Seychelles, western Indian Ocean: Systematics ダ テ ハ ゼ の 社 会 行 動 と 配偶 形 態* and ecology. J. Zool., Lond., 183: 63•`101, figs. 柳 沢 康 信 1•`20. ダ テハ ゼ は ニ シ キ テ ッポ ウエ ビが 掘 っ た巣 穴 を か く Preston, J. L. 1978. Communication systems and れ が と して利 用 して い る.ハ ゼ は 日中巣 穴 の入 口付 近 social interactions in a goby-shrimp symbiosis . を 中心 に活 動 して い るが,繁 殖 期 に は地 表 上 を移 動 し Anim. Behay., 26 (3): 791•`802. て隣 接 個 体 とペ ア を形 成 す る.ペ ア は 通 常2～3日 以 Yanagisawa, Y. 1976. Genus Amblyeleotris (Gobi- 上 維 持 され るが,産 卵 に至 ら ない で別 れ る も の も多 い. idae) of Japan and geographical variations of A. 配 偶 者 獲 得 をめ ぐる競 争 は雄 間 で烈 し く,授 精 に成 功 japonica Takagi. Publ. Seto Mar. Biol. Lab., した と推 測 され る雄 は社 会 的 に優 位 な大 型 個 体 で あ っ 23 (1/2): 145•`168, figs. 1•`11. た.巣 穴 を離 れ て い る時 間,攻 撃 的 出会 い の頻 度,巣 Yanagisawa, Y. 1978. Studies on the interspecific 穴 を所 有 しな い 個体 の割 合 につ い て は,調 査 個 体 群 間 relationship between gobiid fish and snapping に 差 異 が認 め られ た.こ の差 異 は,生 息 地 の 捕 食 圧 と shrimp. I. Gobiid fishes associated with snapping 巣 穴密 度 に 関連 づ け て理 解 で き る こ と を示 唆 した. shrimps in Japan. Publ. Seto Mar. Biol. Lab.,

24 (4/6): 269•`325, figs. 1•`23, pls. 1•`2 . *同 居 関 係 を 結 ぶ ハゼ 類 とテ ッポ ウエ ビ類 の 種 間 関 係 に つ い てIII. (Faculty of Science,Ehime University,2-5 Bunkyocho,Matsuyama 790,Japan) (790松 山市 文 京 町2-5愛 媛 大 学 理 学 部)

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