Japanese Journal of 魚 類 学 雑 誌 Vol. 38, No.3 1991 38巻3号1991年

The Social and Mating System of the Maternal Mouthbrooder moorii (Cichlidae) in

Yasunobu Yanagisawa 1 and Mutsumi Nishida2

Department of Biology, Ehime University, Matsuyama1 790, Japan Department of Marine Sciences, University of the Ryukyus,2 Nishihara, Okinawa 903-01, Japan

Abstract Territorial behaviour, reproduction and migration of the epilithic algal eater, , were investigated in Lake Tanganyika, Africa. Adults of both sexes had individual feeding territories which adjointed each other. Males, who occupied higher rocks than females, usually stayed at the same sites for more than 5 months. Females left their territories to pair with males in the males' territories. Paired females actively foraged under the protection of their mates for up to 3 weeks prior to spawning. After spawning, females usually settled in a site unoccupied by territory-holders to mouthbrood the offspring for a month. An examination of the ovaries and a removal experiment of dominant males suggest that females cannot attain fully mature ovaries in their own territories and choose males whose territories can provide enough food to satisfy their nutritive demand. The evolution of a number of local colour morphs in this is briefly discussed in relation to social selection.

Cichlid in Lake Tanganyika represent one of male's or female's territory or in a spatially separated the most spectacular examples of adaptive radiation spawning site. An understanding of the above for in fishes (Fryer and Iles, 1972; Lowe-McConnell, each colour morph is necessary to understand how 1987; Nishida, in press). Rocky shores in this lake social factors have affected the evolution of colour are inhabited by a huge variety of . morphs.

Rock-dwelling species, whose habitats are disrupted The 'Bemba orange' morph (see Axelrod et al., by sandy beaches, usually include geographical var- 1985, p.502), which is distributed on the north- iants within the lake, which may be incipient species. western shore of the lake, was chosen as the subject

The best-known is Tropheus moorii, which is com- of this study. Fish of this morph could be recognized posed of no less than 20 local colour morphs (Mar- individually from an orange band on the body. Their her, 1959; Matthes, 1962; Nelissen, 1976; Brichard, territorial behaviour, reproductive behaviour and

1978). migration patterns were observed for 5 months so as

The behaviour and ecology of T. moorii have been to clarify their social and mating system. Moreover, intensively studied in aquaria by many workers dominant males were removed experimentally from (Wickler, 1969; Nelissen, 1976) and in the field their territories to determine the manner of resource (Kawanabe, 1981; Takamura, 1983, 1984; Yamaoka, monopolization. 1983; Mbomba, 1986). This fish is an epilithic algal feeder (Takamura, 1983, 1984; Yamaoka, 1983, Methods 1985, 1987), having an individual feeding territory (Kawanabe, 1981). The courtship and spawning Field observations and sampling were conducted behaviour is very similar among colour morphs at Bemba (=Pemba), about 25km south of Uvira

(Wickler, 1969; Nelissen, 1976). Eggs are mouth- (3•‹ 24'S, 29•‹ 10'E), Zaire, with the aid of SCUBA. A brooded only by females (Wickler, 1969). However, 30•~20m quadrat, divided into 5•~5m grids, was set many aspects of social and mating systems of this fish on the rock and sand bottom at a depth of 2.8 to 6.1 in nature still remain to be investigated. For exam- m, where adult T. moorii were abundant. In the ple, little was known about how long each fish main- quadrat, the configuration of rocks was sketched on tains its feeding territory, how consexuals compete a section paper (scale: 3/200) and water depths of the for a mate, and whether mating occurs within the top and base of a rock and the sand floor were

―271― 魚類学雑誌 Japan. J. Ichthyol. 38 (3), 1991

measured at 474 points using a tapeline with a float. and the number of T. moorii in areas measuring 10m

T. moorii larger than 75mm SL in the quadrat long by 2.5m wide on both sides of each line was were individually recognized by using a sketch of the recorded along with their approximate body sizes. Specimens were caught with a small-mesh barrier profile of a vertical orange band on each side of the body, although the exact identification of wandering net and two hand nets. After a small amount of fish was often difficult. They were regularly censused undiluted formalin was injected into their abdonimal during early June and late October, 1987, most in- cavities, specimens were preserved in 10% formalin tensively (usually at intervals of 2-4 days) during 17 within 1.5 hours after collection. Adult fish in the

July and 21 September. In each census, their posi- quadrat were collected during 26 and 31 October

tions and social states (i.e., solitary, paired and after the removal experiment. Outside the quadrat,

mouthbrooding) were recorded. mouthbrooding females were collected intensively.

In the quadrat, behavioural interactions of each In the laboratory, standard length, wet body weight,

fish with conspecifics and other fish species were wet gonad weight, wet weight of fat stored within the

observed twice for 15 min, once during 9 and 23 June abdominal cavity and wet weight of gut contents

and once during 17 September and 6 October. At the (total gut weight-vacant gut weight) were meas-

same time, its exact position was plotted on the map ured. Stomach contents were weighed after heating

every 30 sec. The minimum convex polygon cover- at 60•Ž for 24 hours (dry weight) and again after

ing all points plotted was regarded as its home range. heating at 550•Ž for 4 hours (ash weight), and the

If the border of a fish's moving area was clearly fraction of organic matter {[(dry weight-ash

defined by the substrate (e.g., a cliff of rock) or if a weight)/dry weight]•~100} was calculated.

fish moved between two separated areas, we did not

adhere to the rule of the minimum convex polygon. Results The extent of home range overlap of each fish be-

tween the two periods is given by [2c/(a+b)]•~100, Distribution and home range. T. moorii inhabit-

where c is the overlapped area of home ranges in the ed the bottoms of rocks and boulders shallower than

two periods (a and b). Sex was determined by gonad 18m. They also occurred at mixed zones of rocks,

examination of fish collected and inferred from boulders and sand, but were never seen on a purely

mouthbrooding and pairing in fish not caught. sandy floor. Juveniles smaller than 40mm SL were

On 9 October, five males whom females had fre- almost exclusively found on the bottom of boulders mixed with pebbles at a depth of 0.5-2m (Table 1). quently visited were removed. The behaviour pat- terns of individuals who replaced these males in their Very small juveniles less than 20mm SL, which were

territories were observed for 15 min each, 1, 4 and 15 rarely found in a line census, remained in conceal-

days after removal and for a few minutes 7 days after ment among boulders and pebbles beneath surface

removal. The behaviour of neighbouring fish was boulders shallower than 1m. The smallest juvenile

also observed for 2-15 min. collected was 14.0mm SL, which was of similar size

The distribution of T moorii in relation to water to grown offspring mouthbrooded by the female (the

depth and substrate was recorded on 14 August. maximum size being 15.9mm SL), suggesting that

Three parallel lines, about 100m apart, were set the young settle in such shallow habitats after be-

temporarily from the shore to a site 30 m in depth, coming independent from the parent.

Table 1. Population density (per 100 m2) of Tropheus moorii in relation to water depth. The data from three line censuses are combined. *, purely sandy area is not included.

―272― Yanagisawa and Nishida: Cichlid Social and Mating System

p>0.05). However, it was positively correlated with the area of rocks in the home range of males (r=

0.445, n=50, p<0.01) and nearly so for females

(r=0.292, n=43, p•à0.05). Adults had on average 3.7 neighbours within 1m of

their home range boundaries. The relative frequency

of neighbours being of the opposite sex was greater

than that expected from random distribution (male- male 89, male-female 228, female-female 43; x2=

29.74, p<0.001). This distribution pattern suggests

spacing out between consexuals. Except for one

small male (79.8mm SL) and one small female (78.5

Fig. 1. The maximum height of rocks in a home mm), who were often attacked by neighbours and

range for male and female Tropheus moorii. shifted from place to place within a certain area, all

Sample size in parentheses. Data from June and adults defended their home ranges against conspe- September-October are combined. Striped areas cifics and some other cichlid fishes. Their home indicate individuals larger than the average body ranges, therefore, could be regarded as territories. size (97.2mm SL for males and 87.8mm SL for Territorial behaviour. Aggressive and aggression- females). The height is significantly greater in males (Mann-Whitney U test, U1=862, p< inhibiting behaviour patterns between territorial fish 0.01). The female who had the highest value were principally the same as those observed in an lived in a narrow area at the edge of a big rock aquarium (Nelissen, 1976). Attacks by one territo- occupied by two males. rial fish against conspecific territory-holders occur-

red 6.1 times per hour (in 29.5 h observations) and

accounted for 82% (147/180) of all agonistic en-

Adults were abundant in the rocky area up to 8m counters between them. Other aggressive behaviour depth (Table 1). The sex ratio was nearly 1: 1 (29 patterns were the approaching of one fish (12%) and males and 32 females in June, 26 males and 28 confrontation at territory borders (3%). The ap- females in September-October, in the quadrat; x2= proaching of one fish was often followed by the re-

0.148, 0.074, df=1, p>0.05). The mean standard cipient submissively quivering its tail (82%, 18/22). length of males was larger than that of females (x•} All observed attacks, except one, between individuals

SD=97.2•}6.3mm, n=30 vs 87.8•}4.1mm, n=32, of known body size were made by the larger indi- t-test, t=6.89, df=60, p<0.001, for specimens in vidual against the smaller (91/92), and 91% (83/91) the quadrat; 95.7•}6.8mm, n=47 vs 82.8•}5.9mm, of the attacks were between individuals with a size n=89, t=11.5, df=134, p<0.001, for all speci- difference of more than 5mm SL. Attacking inter- mens). Home ranges of two neighbouring fish ad- actions between sexes were more frequent than those

between consexuals (male-male 29, male-female 71, joined, scarcely overlapping with each other except when belonging to paired individuals. Males inhab- female-female 24). This result may simply reflect ited much larger home ranges than females (6.1•}2.8 the distribution pattern of T. moorii in that neigh- m2, n=55 vs 3.4•}2.1 m2, n=53; t=5.65, df=106, bours were disproportionately of the other sex. In p<0.001, data of June and of September-October every attacking interaction between sexes, the at- combined). tacker was a male.

Most of the large and high rocks were occupied by Territorial fish also attacked nonterritorial con- males. Accordingly, the area of rocks in a home specifics when their territories were invaded. Attacks range, measured in horizontal projection on the map, by males against invaders were more frequent than was much greater for males than for females (3.92•} those by females (2.2 vs 1.3 per hour). The invaders,

2.26 m2, n=50 vs 1.58•}1.20 m2, n=46; t=5.51, whose sexes could not usually be identified, were df=94, p<0.001) and the average maximum height generally smaller than the territorial fish. Some of of rocks in a home range was also greater for males them were wandering unpaired females. The verti-

(Fig. 1). The body size of the fish was not correlated cal, orange band of the invaders was usually faded. with the home range size among either males (r= Tettitory-holders sometimes followed invaders with-

0.07, n=50, p>0.05) or females (r=0.10, n=43, out attacking until the latter had left the territory.

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Males sometimes accepted invaders by courtship categorized as paired or solitary, and those of the movements, leading and quivering. female as paired, solitary or mouthbrooding. Pair Attacking was also directed to 18 heterospecifics formation always involved a female's migration to a (3.9 per hour), all of which were cichlid fishes. male's territory where the pair was maintained. Attacks against a congeneric fish Pairs which broke up by the next census or in which (25%) and a scale-eater Perissodus microlepis (17%) the male did not consort with the female (see below) were often fierce but those against the other fishes were regarded as tentative. Females carrying ferti- were usually mild. lized eggs in their mouths always left the males' Movement. About half of the adults in the quad- territories. rat kept their territories at the same sites throughout Changes of social states for males, who paired the study period between June and September- with a female at least once, and for females, who are October and the others moved elsewhere or disap- estimated to have reproduced, are shown in Figs. 2 peared (Table 2). The proportion of individuals who and 3, respectively. maintained their territories at the same sites was 1) Pair formation. Fifty-one individuals were much higher in males (83%) than in females (28%), found in male territories at least once during quadrat and among these residents the degree of territory censuses. Of them, 13 had formerly been solitary in overlap between the two periods was greater in males the quadrat, 4 were in male territories from the start (68.0+16.4%, n=23 vs 46.9+16.7%, n=9; Mann- of the census, and the other 34 came from outside. Whitney U test, U1=39, p<0.01). Sixteen of the first two groups were finally collected Of 5 males who did not stay at the same site, 2 and ascertained to be 14 females and 2 males. The shifted 3 and 10m, respectively, one occupied a distance between the female's original territory and neighbouring territory from which a male had dis- the male's territory to which she moved ranged from appeared and the other, which had been on the sandy 1 to 15m (4.7+3.8m, n=11; distance between the bottom with small rocks, moved outside the quadrat. centres of the two territories). In 7 out of 14 cases, The whereabouts of the other 3 males after the the migration was to the neighbouring territory. disappearance remained unknown. Of 23 females Females in the male territory were 'fickle' until who did not stay at the same site (Table 2), move- they paired stably with one male. Some females ments of 19 females were related to pairing and returned to their original territories after a short stay brooding (see below). The other 4 females moved 3- in a male's territory and some others visited two or 15m to settle into sites from which territory-holders more territories in succession. Two typical cases of had disappeared (2 cases) or sites which were un- successive visits are detailed below. occupied by territory-holders (2 cases). One female, who came from outside the quadrat, On the other hand, 63 individuals were new ar- visited three males (M7, M22 and M19) staying in rivals in the quadrat during the study period. When each territory for 2, 20 and 6 min, respectively, we found them for the first time, 34 were paired with during a 35 min observation period. Two days later males in the males' territories, 12 were singly mouth- she again visited these males (6, 25 and 6 min), as brooding, and 17 were solitary without mouth- well as three other males outside the quadrat (1, 3 brooding. More than half of them had disappeared and 9 min), in a 75 min observation. Another female from the quadrat by the next census; only 11 stayed (F3), who had been a territory-holder, was found in in the quadrat for more than 2 weeks. one of four male (M4, M5, M6 and M7) territories Reproduction. Social states of the male were in six successive censuses. These territories were

Table 2. The residence and movement of adult Tropheus moorii who were found in the quadrat from June 1987 until September-October 1987. *, 6 returned to their original territories by September-October after having left the territories for reproduction.

―274― Yanagisawa and Nishida: Cichlid Social and Mating System

Fig. 2. Changes of social states for male Tropheus moorii who have paired with females at least once. Num- bers following M are individual numbers. Social states were categorized as: solitary (puls sign), tentatively paired (open triangle) and stably paired (solid triangle). Underlined solid triangles indicate pairing with a male (see text). A minus sign indicates absence from the quadrat . Social states of M9 and M29 are shown on the same line, because we could not specify the exact day on which the latter replaced the former (occurred in the second half of August).

Fig. 3. Changes of social states for female Tropheus moorii who are estimated to have reproduced. Numbers following F are individual numbers. Social states were categorized as: solitary (plus sign), tentatively paired (open triangle), stably paired (solid triangle) and mouthbrooding (open circle). A minus sign indicates absence from the quadrat.

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within 8m of her territory. When visiting each male, 2) Spawning and brooding. In a stable pair, she was never attacked by him. After a short stay pseudo-spawning' (Nelissen, 1976) between ' the male and female sometimes occurred at a particular (usually less than 10 min), she returned to her ter- ritory or moved to another male's territory. part of the territory. Such a site was usually a flat stone or rock whose upper surface was smooth and The male usually received a visiting female with

the tail-quivering courtship behaviour. He usually gently sloped in the shade of a big rock. Actual spawning was observed on one occasion. The se- followed her around (usually within 50cm) wher-

ever she went in his territory (this behaviour is quences of courtship and spawning behaviour were

referred to as consortship hereafter), although some conducted in the same manner as those observed in

males merely tolerated the presence of a female, an aquarium (Nelissen, 1976).

showing neither aggressive behaviour nor consort- Of 20 females who had been stably paired with males during two or more successive consuses, 12 ship. The female with whom the male consorted

devoted herself to foraging, her feeding rate being were found to be mouthbrooding and the other 8 had

very high (see the next section). disappeared in the following censuses. Of the 8 females who had disappeared, 2 (F4, F15) reappear- Of 29 territorial males in the quadrat, 19 were

visited by females at least once. However, only 12 of ed after an absence of 44 and 67 days, respectively, at

them formed stable pairs with females that lasted the sites of their original territories. They were

niore than 2 successive censuses (Fig. 2). The du- solitary and not mouthbrooding when they reap-

ration of stable pairing varied a great deal among peared. Their absence was longer than the mouth- brooding duration (about 33 days, Yanagisawa and pairs (Fig. 3), ranging from less than 4 days to 21 days. The average body size of males who formed Sato, 1990), suggesting that they had mouthbrooded

stable pairs was not significantly greater than that of somewhere else in this period. The fact that females

the other territorial males (98.7•}4.4mm SL, n=11 who had once stably paired were always found to be

vs 96.5•}6.9mm SL, n=18; t=0.93, df=27, p= mouthbrooding indicates that the formation of a

0.36). A male (M23, 94.4mm) who formed pairs stable pair is followed by spawning. Mouthbrooding females were always solitary, most frequently was a little smaller than the average

male body size (97.2mm), and the largest male in outside the males' territories, except for one female

the quadrat (M19, 105.0mm) never formed a stable who was found under a rock in the male's territory in the first census after spawning. She disappeared pair (Fig. 2). Males who formed stable pairs with females generally held territories including a high before the next census. The average distance be-

rock and a wide rocky area. Neighbouring males, by tween the males' territories where females had paired

contrast, never formed stable pairs, even if their and sites where they were mouthbrooding in or

territories also included a high rock and a wide rocky around the quadrat was 4.7m (range: 2-11m, n=

area. 12). The actual average distance may be greater,

Pairs between males appeared on two occasions since mouthbrooding females who had gone far away from the quadrat were not considered. Three fe- (between M10 and M1 and between M26 and M23, Fig. 2). In each case, two males had been neigh- males (F1, F5, F26) returned to their original terri-

bours, with one subsequently moving to the other's tories to mouthbrood. (F5 was solitary without

territory. The visitor was smaller in body size in one mouthbrooding in her territory until 20 July but was mouthbrooding in her territory in the next census on case (82.5 vs 97.8mm SL), but larger in the other 25 July. Therefore, the territory in which she - (101.4 vs 94.4mm SL). The homosexual pairs continued for 2 and 6 successive censuses, respec- ed is unknown.)

tively. The resident male consorted with the visitor Mouthbrooding females usually settled in a site

in the same manner as in a heterosexual pair. After unoccupied by territory-owners; the sand-rock in-

the breakup of the pair, the latter returned to his terface was often used. They were inactive on the

original territory and remained solitary until the end bottom and their home ranges were small (0.75•}

of study. In both cases, the visitor's own territory 0.48 m2, n=3). They were aggressive only against

included a much smaller rocky area than the terri- small fishes such as subadults of Tropheus moorii and T. duboisi. One exception is a female (F25) who tory to which he visited (0.80 vs 3.14, 0.84 vs 7.12

m2) and the maximum height of rocks in his territory actively defended her territory against intruders.

was lower (10 vs 35, 40 vs 65cm). Females took no food into the gut throughout the

―276― Yanagisawa and Nishida: Cichlid Social and Mating System

mouthbrooding period, although their browsing rate increased with the need to feed the young developing in the buccal cavity (Yanagisawa and Sato, 1990).

Temporal feeding of grown young outside the female's mouth, which commonly occurs in mouth- brooding cichlid fishes (Fryer and Iles, 1972), was never seen in this study, though it was observed in an aquarium. Juveniles soon after independence from the mother were never found in the quadrat, but in shallower water. On 2 occasions, a female mouth- brooding young (more than 30-day old) in the quad- Fig. 4. Frequency distribution of gonadosomatic index (GSI) for mouthbrooding females and rat was absent from her brooding site, and had nonbrooding females in Tropheus moorii. Black probably migrated to a shallower area to release the areas are for females paired in a male territory. young. After mouthbrooding, females usually re- Sample size in parentheses. mained at the brooding sites (n=14), but a few fe- males moved slightly (1, 2 and 6m, n=3). They expanded their territories as their feeding activity responding to the higher feeding rate, females with increased. whom males consorted had higher values of this

Of 32 females who stayed in the quadrat at the index than the consorting males (6.63•}1.05, n=7 vs start of the study, 18 spawned during the study 4.87•}1.20, n=7; t=3.12, df=12, p<0.01). period (Fig. 3), if females who disappeared after The fraction of organic matter in the stomach stable pairing were regarded as having spawned. contents varied greatly between individuals, but did

Two (F15, F30) of them spawned twice. The other not differ significantly between males (24.8•}7.5, n=

14 females never spawned. 25) and females (25.8•}9.2, n=27). Individuals

Feeding activity and some physical conditions. occupying large rock outcrops protruding more than

T. moorii spent most of the time browsing epilithic 1m had higher values of organic matter than those algae within the territory. The feeding rate (the occupying the lower rocks (30.4•}4.8, n=8 males+ number of browsing actions per 5 min) of a solitary 8 females vs 21.7•}8.2, n=17 females+19 females; male did not differ from that of a nonbrooding, t=3.79, df=42, p<0.001). Females with whom solitary female (x•}SD=179.0•}21.2, n=8 vs males consorted usually had larger values than the

162.7•}49.5, n=23; Mann-Whitney U test, U1= other females, but the differences were not significant

63.5, p>0.05). On the other hand, in a pair wherein (30.5•}9.9, n=7 vs 24.1•}8.3, n=20; t=1.61, df= a male consorted with a female, the female always 25, p=0.12). fed more actively than her mate (266.4•}33.9 vs Gonadosomatic index [(wet gonad weight/ wet

149.5•}34.9, n=10; Wilcoxon signed rank test, T= body weight)•~100] was high in females with whom

0, p<0.01). The feeding rate of such females was males consorted (3.74•}0.86, n=7; Fig. 4); they had higher than that of solitary females (Mann-Whitney fully mature ovaries. In contrast, this index was

U test, U1=12.5, p<0.001), and conversely, that of much lower in mouthbrooding females (0.56•}0.28, the consorting males was nearly significantly lower n=39); none had mature eggs in the ovaries with the than that of solitary males (U1=7.5,p•à0.05). exception of one individual whose ovary contained a

Females mouthbrooding early embryos rarely single mature egg. Gonadal recovery of females showed feeding actions, but their feeding rate in- after mouthbrooding was slow: no females who were creased with the development of young, as already known to have passed 25-90 post-mouthbrooding reported (Yanagisawa and Sato, 1990). Food taken days had fully mature eggs, and their gonadosomatic in the mouth was not swallowed, but ingested by the index remained low (0.54•}0.26, n=14). This low young in the buccal cavity (Yanagisawa and Sato, gonadosomatic index was common to most solitary 1990). females (Fig. 4). These results suggest that the

Gut fullness index [(wet weight of gut contents/ ovaries rapidly develop in females during the period wet body weight)•~100] did not differ between sol- that they are in the male's territory. Gonadosomatic itary males and females (5.48•}1.72, n=38 vs 5.89•} index of males was constantly low (0.13•}0.05, n=

1.48, n=39; t-test, t=1.36, df= 75, p=0.18). Cor- 47).

―277― 魚類学雑誌 Japan. J. Ichthyol. 38(3), 1991

a

b

c

d

e

Fig. 5. Positional changes of Tropheus moorii 1, 4 and 15 days after the removal of the dominant males, M22 (a), M23 (b), M5 (c), M7 (d) and M25 (e). M not followed by a numeral indicates a male of unknown origin. Each territory was estimated from a 15 min observation of removed and replacement fish and from a 2-15 min observation of other fish.

The condition factor {[(wet body weight-wet condition factor of males (4.32•}0.32, n=34) was

weight of gut contents)/(standard length)3] •~ 100} similar to that of nonbrooding solitary females and

of mouthbrooding females was lower than that of did not correlate with their social states.

nonbrooding solitary females (4.06 g/mm3•}0.24, The amount of fat stored within the abdominal

n=39 vs 4.37•}0.23, n=39; t-test, t=5.81, df=76, cavity varied greatly between individuals; fat index

p<0.001). Females with whom males consorted [(wet fat weight/wet body weight) •~ 100] ranged surpassed nonbrooding solitary females in this factor from 0 to 4.41. The average fat index of males was much higher than that of females (1.07•}1.00, n= (4.63•}0.23, n=7; t=2.77, df=44, p<0.01). The

―278― Yanagisawa and Nishida: Cichlid Social and Mating System

37, vs 0.39•}0.58, n=65; t=4.27, df=100, p< and consorted with a female of unknown origin. 0.001), suggesting that surplus nutrition is stored in From the 5th day onwards, he remained solitary, and the form of fat in the male. Among males whose his territory nearly coinciding with the former M7 reproductive experiences were known, those who territory. had not spawned throughout the study period had 5) Removal of M25 (100.4mm, Fig.5e): A higher values of this index than those who had male (91.3mm) of unknown origin and F24 (87.4 spawned (Mann-Whitney U test, N1=15, N2=11, mm), who had been at the verge of M25's territory, U1=43, p<0.05). In the female, fat index did not each occupied a part of M25's territory within a day correlate with the social states. of the removal. By the 5th day, both had expanded Removal experiment. After the removal of 5 their territories dividing M25's territory into equal males (M22, M23, M5, M7, M25) whom females shares. However, at this time the male was acci- had often visited, all of their territories were replaced dentally caught with a barrier net. Further expan- by one or two conspecifics. The behaviour of the sion of the territory by F24 did not occur thereafter . replacement fish is individually described below. Thus territories of removed males were finally 1) Removal of M22 (104.0mm, Fig.5a): Within occupied by adjacent males (in 3 cases) or males of one day of the removal, two neighbours, M20 (102.6 unknown origin (in 2 cases). These males paired mm) and F26 (98.1mm), expanded their territories with females within a week of the replacement, occupying two thirds and one third of M22's terri- except in experiment 5 where the replacement male tory, respectively. From the 5th day on, F26, who was captured by accident, and two of them spawned had withdrawn from M22's territory, stayed within or are thought to have spawned with new mates. her original territory, whereas, M20, who had left his Three replacement males whose previous states were original territory, managed all of M22's territory. known had never paired (M20, M24) or only ten- On the 8th day, M20 was paired with a female. tatively paired (M6) with females in their original 2) Removal of M23 (94.4mm, Fig.5b): One territories, though they were as large as the removed day after the removal, a neighbouring male, M24 males.

(97.5mm), dominated a wide area including both M23's territory and his original territory. F27 (90.6 Discussion mm), who had been paired with M23, remained in

the territory after the latter's removal. M24 some- Social and mating system. Most cichlid fishes in times consorted with her. On the 5th day, M24 still African lakes are maternal mouthbrooders, in which had a large territory at the same site and sometimes the female broods eggs and young in her mouth and consorted with F27 (105 sec during a 15 min period). the male has no concern with brooding (Fryer and On the 8th and 16th days, F27 kept still at the border Iles, 1972; Lowe-McConnell, 1987). Such maternal of M24's territory while mouthbrooding, suggesting mouthbrooders are common in Lake Tanganyika, that she had spawned with M24. By the 16th day, although one third of the cichlid species in this lake M24's territory had contracted, to almost coincide are substrate brooders (Brichard, 1978) and some of with the former M23 territory. the mouthbrooders are biparental, with both male 3) Removal of M5 (101.3mm, Fig.5c): Within and female participating in mouthbrooding and/or a day of the removal, F3 (86.0mm), who had been guarding on the substrate (Yanagisawa and Nsh- lost for a week, appeared in one corner of M5's ombo, 1983; Yanagisawa, 1986; Kuwamura, 1986, territory. She remained there until she was collected 1988; Kuwamura et al., 1989; Yanagisawa et al., 20 days later. By the 5th day, a neighbouring male, 1990). M6 (101.2mm), had expanded his territory to in- The mating system of maternal mouthbrooders of clude the main part of M5's territory unoccupied by African cichlid fishes so far studied is usually pro- F3. While maintaining a large territory, M6 paired miscuous: a male and female do not form a lasting with a female of unknown origin on the 8th day and pair bond and both breed more than once with spawned with her on the 16th day (this is the only different mates. A common feature is that the female spawning we could observe). visits the male's territory to spawn and leaves car- 4) Removal of M7 (98.0mm, Fig.5d): Within a rying fertilized eggs inside the mouth soon after the day of the removal, a male (100.0mm) of unknown spawning (Kuwamura, 1986). The male's territory origin occupied the greater part of M7's territory is established for mating in many species, such as

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Cyathopharynx furcifer (Nshombo, 1991), Astato- display, she often left his territory within a few burtoni (Fernald and Hirata, 1977) and Cyr- minutes. Eventually, she formed stable pairs with tocara eucinostomus (McKaye, 1983). Alternatively, some particular males. Such behaviour suggests that the territory is the one which the male has maintain- females assess the quality of the territory and/or male ed as a feeding site, as seen in Pseudosimochromis during the stay in the male's territory. There was curvifrons (Kuwamura, 1987) and only a weak correlation between the body size of zebra (Holzberg, 1978; Ribbink et al., 1983) as well males and their success of pairing, and replacement as in T. moorii. males in the male removal experiment, who had long Peculiar to T. moorii as a maternal mouthbrooder been solitary in their old territories, soon got mates. is that a male and female form a pair bond for several Thus the quality of the territory may be the more days prior to spawning and the female actively for- important criterion for mate choice by the female, ages while the male consorts with her. Ecological and may depend upon the availability of food. conditions which make this behaviour beneficial A remarkable feature of male T. moorii is that they should be considered. are strongly site-attached, irrespective of their re- In T. moorii, the gonadosomatic index was low in productive achievement. Most males remained in almost all solitary females (Fig.4) and the gonadal their territories throughout the study, even if they recovery of solitary females after the termination of had never received visits from females. Fat was mouthbrooding was very slow. These facts suggest stored more in bachelor males than in males who that females do not attain fully mature ovaries in experienced stable pairing. From this result we their own territories in spite of continuous daytime suggest that the bachelor males feed in their terri- foraging. Epilithic algae, the primary food item for tories so as to get as much nutrition as possible until T. moorii, are not homogeneous in distribution as they acquire a territory that attracts females. formerly believed (Power, 1983; Reinthal, 1990); The unusual behaviour of two males (M10, M26), their abundance and species composition vary cor- who stayed in territories of neighbouring males for responding to depth, and substrate inclination, etc. several days, may be explained from the standpoint Furthermore, the efficiency of dietary carbon and of the improvement in their nutritive conditions. nitrogen conversion to growth by some herbivorous Curiously, the resident males not only tolerated their fishes is extremely low (Polunin and Brothers, 1989) presence but also consorted with them. Possibly the and deficiency of minerals and trace elements dras- resident males erroneously regarded the 'changers-on' tically lowers fecundity (Luquet and Watanabe, as females. 1986). We, therefore, infer that the female's terri- Colour morphs and social selection. Colour dif- tory is a second-grade, feeding site where some nu- ferences between local populations are a notable tritive elements are in short supply. Consequently feature of cichlid fishes in Lake Tanganyika. This the female makes up for the deficiency prior to feature is most remarkably represented by T. moorii, spawning by devoting herself to foraging under the in which many local morphs have distinct colour male's protection. patterns (Brichard, 1978; Axelrod et al., 1985; The increased feeding rate of a paired female and Konings, 1988). For example, the •eBemba orange' the attentive defense by her mate, as seen in T. morph, which we studied, has a greatly different moorii, are also known in monogamous butterfly- body colour from the more northern •eAll black' fishes, Chaetodon multicinctus and C. quadrimacu- morph, which has no band, although the two popu- latus, which feed on corals, also an energetically poor lations are separated only by a sandy beach a few food resource (Hourigan, 1989). The hypothesis kilometers long. regarding the selective advantage of the pair bond It is unlikely that such colour differences resulted for these bufferflyfishes is that fecundity is food only from natural selection, since great geographical limited and pairing increases the time available to variation in the environmental conditions corre- females for feeding and enables the paired male to sponding to the colour variations apparently does not share in his mate's increased fecundity (Hourigan, exist in the habitat of T. moorii. However, if body 1989). This idea may be applicable to T. moorii. colour is used as a highly significant signal in social Each female usually visited more than one male's interaction and selection for success in the competi- territory before the formation of a stable pair. Even tion using this signal is intense, then a rapid diver- if a male received the visiting female with a courtship en in in body colour can be expected between iso-

―280― Yanagisawa and Nishida: Cichlid Social and Mating System

lated populations, despite a lack of environmental

differences (see West-Eberhard, 1983; Dominey,

1984). The possibility that T. moorii uses the body Literature cited

colour as a social signal is briefly considered below. Axelrod, H.R., W.E. Burgess, N. Pronek and J.G. Walls. The bright, vertical band on the dark body is 1985. Dr. Axelrod's atlas of freshwater aquarium fishes. conspicuous in the 'Bemba orange' morph, as well as TFH Pub., Neptune City, 782pp. in many other morphs. In this morph, the band is Brichard, P. 1978. Fishes of Lake Tanganyika. TFH Pub., orange in both males and females, though usually a Neptune City, 448pp. little more yellowish in the latter, with a longer and Dominey, W.J. 1984. Effects of sexual selection and life

broader continuation onto the . Since there history on speciation: species flocks in African

is little sexual dichromatism and no marked colour and Hawaian Drosophila. Pages 231-249 in A.A. Ech-

changes occur during courtship and spawning, body elle and I. Kornfield, eds. species flocks.

colour seems to be unimportant in mate choice. University of Maine at Orono Press, Orono. Fernald, R.D. and N.R. Hirata. 1977. Field study of On the other hand, it is clear that the body colour Haplochromis burtoni: quantitative behavioural observa- serves as a signal in social behaviour. As this study tions. Anim. Behay., 25: 964-975. showed, nearly all of the hard substrates in the Fryer, G. and T.D. Iles. 1972. The cichlid fishes of the habitat were packed with individual territories, each Great Lakes of Africa. Oliver & Boyd, Edinburgh, 641 being stably maintained for a long time. The orange pp. band of territory-holders sometimes became brighter Holzberg, S. 1978. A field and laboratory study of the when they attacked intruders. In contrast, the band behaviour and ecology of Pseudotropheus zebra (Boulen- usually faded in fish who left their own territories, ger), an endemic cichlid of (Pisces; Cich-

unless chasing intruders. Such colour changes may lidae). Z. Zool. Syst. Evolut.-forsch., 16: 171-187.

enable each fish to inform others about the level of its Hourigan, T.H. 1989. Environmental determinants of butterflyfish social systems. Env. Biol. Fish., 25: 61-78. aggressiveness and may therefore serve to reduce Kawanabe, H. 1981. Territorial behaviour of Tropheus agonistic encounters. Moreover, body colour may moorei (: Cichlidae) with a preliminary serve for personal acquaintances between neigh- consideration on the territorial forms in . Afr. bouring individuals established through frequent Stud. Monogr., 1: 101-106. contacts during territorial and extraterritorial ac- Konings, A. 1988. Tanganyika cichlids. Verduijn Cichlids, tivities (C. Sturmbauer, pers. comm.). Zevenhuizen, 272pp. Our preliminary observations of the •eAll black' Kuwamura, T. 1986. and mating systems of morph, whose colour change was not distinct, indi- cichlid fishes in Lake Tanganyika: a preliminary field cate that it more frequently made one-sided attacks survey. J. Ethol., 4: 129-146. and less frequently performed appeasement displays Kuwamura, T. 1987. Male mating territory and sneaking compared with the •eBemba orange' morph. The in a maternal mouthbrooder, Pseudosimochromis curvi- difference in colour pattern between these two frons (Pisces; Cichlidae). J. Ethol., 5: 203-206. Kuwamura, T. 1988.Biparental mouthbrooding and guard- morphs may reflect differences in social and mating ing in a Tanganyikan cichlid Haplotaxodon microlepis. systems. Comparative studies on the social and Japan. J. Ichthyol., 35: 62-68. mating systems of different colour morphs will be Kuwamura, T., M. Nagoshi and T. Sato. 1989. Female- fruitful for understanding of how the body colour is to-male shift of mouthbrooding in a cichlid fish, Tanga- used as a signal in social competition in this fish. nicodus irsacae, with notes on breeding habits of two related species in Lake Tanganyika. Env, Biol. Fish., 24: 187-198. Acknowledgments Lowe-McConnell, R.H. 1987. Ecological studies in trop-

We thank H. Kawanabe for his invaluable advice. ical fish communities. Cambridge University Press, Cambridge, 382pp. We also thank N. Zana, M.K. Kwetuenda, M.M. Luquet, P. and T. Watanabe. 1986. Interaction "nutri- Gashagaza, M. Nshombo and other members of tion-reproduction" in fish. Fish Physiol. Biochem., 2: C.R.S.N., Zaire, who offered the use of their facilities 121-129. and assistance for the field work. This study was Marlier, G. 1959. Observations sur la biologie littorale du supported by the Japan International Cooperation lac Tanganika. Rev. Zool. Bot. Afr., 59: 164-183. Agency (No. 4860445) and the Ministry of Educa- Matthes, H. 1962. Poissons nouveaux ou interessants du tion, Science and Culture, Japan (No. 63041080). Lac Tanganika et du Ruanda. Annal. Mus. R. Afr.

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