Japanese Journal of Ichthyology 魚 類 学 雑 誌32巻1号1985年 Vol.32,No.11985

Scale-Eating in Perissodus microlepis(Cichlidae)and Change of Its Food Habits with Growth

Muderhwa Nshombo,Yasunobu Yanagisawa and Makoto Nagoshi Received August 21,1984) (

Abstract Scale-eating behaviour of Perissodus microlepis was observed in its natural habitat and the stomach contents of individuals at various developmental stages were examined.Young guarded by the parents fed on zooplankters,and juveniles exploited a wide variety of food items: zooplankters,phytoplankters,benthic and scales of other fishes.Adults subsisted pri- marily on scales.Adult P.microlepis removed scales from diverse fish ,most intensively from algae-eating larger than themselves and with flat bodies.Most of their attacks were delivered from near the substrate.They sometimes ambushed their prey using the underside or crevice of a rock as cover.Fishes engaging in feeding,territorial attacking or courtship display were often attacked.

The cichlids of the African lakes exhibit a of Uvira,Luhanga and Mpemba situated at the great diversity of feeding habits(Fryer,1959; northern end of during the Greenwood,1964;Fryer and Iles,1972).Scales period from August to November 1981,in Feb- of living fishes are exploited by some cichlids ruary 1982 and from August to November 1983. endemic to Lake Victoria,Lake Tanganyika or SCUBA was used in all observations and collec- Lake Malawi,indicating that the scale-eating tions.Adult P.microlepis floated in midwater habit has independently evolved several times or wandered near the substrate shallower than (Fryer and Iles,1972).Perissodus microlepis 20 m.Floating adults were usually less active is one of the seven species known as scale- in scale-eating.Fifty nine adults wandering eaters in Lake Tanganyika(Poll,1956;Liem and near the substrate were followed and observed Stewart,1976).Brichard(1978)and Kawanabe for 60 min,keeping 2-5 m from them.When (pers.comm.)observed scale-eating behaviour they succeeded in removing scales from prey of this fish in the field.The latter observed fishes,the sites from which they started a dash that it succeeded in ripping off scales from prey and the situations of the prey fishes just prior to fishes when they were busy in territorial attacking being attacked(e.g.,solitary or schooling,or or sexual display.However,no quantitative moving or stationary)were recorded.The sites observation has been carried out on the be- were categorized into midwater and substrate, haviour of P.microlepis and their prey. and the latter was still divided into six categories: In the present study,we observed quantita- the top,lateral side,underside and crevice of a tively the scale-eating behaviour of adult P. rock,the ravine between rocks,and the other microlepis and situations and reactions of prey substrates(stones,gravel,sand and so on).We fishes when they were attacked.Prey-species sometimes could not identify species of Petro- preference by P.microlepis was also analyzed, chromis,Ophthalmotilapia and for comparing the numbers of observed attacks on certain in the field,so those of each were respective species with their relative densities lumped.To estimate the prey-species preference in the field.Stomach contents of this fish at by P.microlepis,the numbers of cichlids in a various developmental stages were examined to 20 x 20 m2 quadrat(0-12 m depths)at Luhanga analyze the degree of specialization of its food counted by the Japanese team in January and habits. February 1980(Hori et al.,1983)and December 1983(unpublished data)were used as the rela- Materials and methods tive densities of prey fishes in the study areas. The field work was carried out at rocky shore Specimens of P.microlepis were collected with

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Table 1.Sites from which Perissodus microlepis started a dash to attack prey fishes .

hand-nets and a gill-net.Stomach contents of Barilius moorei(Cyprinidae).Attacks on 207 non-brooding adults and juveniles and 93 cichlids amounted 89 percent of the total.The young guarded by the parents were examined. epilithic algae-eaters moorei and To analyze them,the occurrence method and, spp.were most frequently attacked, in part,the number method were used. followed by Ophthalmotilapia spp.and L.tan- Caloric value of scales was measured with an ganicanus hovering near rocks. oxygen bomb calorimeter by using scales from To estimate a prey-species preference by P. two (89 and 93mm SL), microlepis,the numbers of adult cichlids in the two Tropheus moorei(73 and 79mm)and three quadrat at Luhanga were compared with the Cyathopharynx furcifer(81,86 and 106mm). numbers of attacks observed(Table 2).The numbers of non-cichlids in the quadrat were not Results available.Frequencies of observed attacks on Scale-eating behaviour.Adult P.microlepis cichlid species of smaller body sizes than adult wandered above rocks,moving 20 to 70 m in P.microlepis were much lower than expected an hour.They succeeded in striking at prey when it is presumed that the frequency of attacks fishes 853 times during the 3,200 min observa- on each species are in proportion to its relative tion period.P.microlepis stealthily approached density(Table 3).A small species Lamprologus its prey or ambushed.Just prior to making an brichardi,which swarmed near rocks,though attack,it usually stopped for a moment at a amounting to 71 percent of all cichlids in number, particular site and directed its head towards the was only rarely attacked(7 percent of the total). prey.Dark stripes on its body faded before Small benthic fishes, bifrenatus attacking,resulting in the reduction of con- and T.temporalis,were also very common but spicuousness.It dashed horizontally or slightly were very rarely attacked(Table 2).Among upwards and struck at the flank of the prey from cichlids whose adults were larger than,or as a perpendicular or posterior position.The large as,adult P.microlepis,those with great dislodged scales,if scattered in the water,were body depths were selectively attacked(Table 3). immediately picked up as they sank.The Omnivorous cichlids,including pelagic species length of a dash was between 20 and 200 cm. Ophthalmotilapia spp.,seem to have been selec- Sites from which it started a dash are shown tively attacked(Table 3),but this elucidation is in Table 1.Seventy five percent of attacks were probably not true because the densities of pelagic from the substrate,though it stayed on the sub- fishes are apt to be underestimated owing to strate only 66 percent of the observation period. their cautiousness.When herbivorous and It frequently started a dash from the top or carnivorous cichlids are compared,the former lateral surface of a rock after approaching the were more frequently attacked relative to their prey along the rock surface.The undersides densities(Z2-10.8,P <0.01).Of 15 species and crevices of rocks or the ravines between which suffered no attack,14 were carnivorous. rocks were sometimes used as cover for ambush. Attacks on Lobochilotes labiatus,Gnatho- Twenty three species and species-groups chromis pfefferi and Lamprologus callipterus, suffered attacks by P.microlepis(Table 2).Only which were cruising individually or more often four are non-cichlid:Lamprichthys tanganicanus in a group in a wide area(Hori,1983),were fre- (Cyprinodontidae),Lates microlepis(Centro- quent relative to their densities,though they pomidae)and Varicorhinus tanganicae and are carnivorous.Carnivorous cichlids Lampro-

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Table 2.Frequencies of attacks by Perissodus microlepis on prey fishes and their adult sizes A,>130mm SL;B,80-130mm;C,<80mm),body depth rates(L,>30% of (SL; S,<30%),food habits(H,herbivorous;0,omnivorous;C,carnivorous)and relative densities in the field.

logus furcifer,L.leleupi and dividuals.Solitary individuals passing in front marlieri,which remained close to the rock sur- of P.microlepis were most commonly attacked. face and frequently retreated into a hole or The territorial algae-eaters Tropheus moorei and crevice,were never or very rarely attacked.P. Petrochromis spp.were often attacked while microlepis never attacked conspecifics(Table 2). they were feeding or chasing intruders.A male Situations of prey fishes when attacked by of Lamprichthys tanganicanus leading a female to P.microlepis are shown in Table 4.One-fifth its spawning site(a narrow crevice of rock)was of the attacks were directed to schooling in- a good attack objective for P.microlepis.

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Table 3.Prey-species preference by Perissodus microlepis in relation to body sizes,body depth rates and food habits of prey fishes.Expected values are set in proportion to the relative densities in the field.

Table 4.Situalons of prey fishes when attacked by Perissodus microlepis.

Prey fishes,however,never let the scale-eater Young fishes smaller than the scale-eater often do as it liked.They took precaution against its showed a defensive display against it by ex- approach.When they witnessed it in the panding the unpaired fins.P.microlepis being vicinity,they either drove it off or kept away detected by prey fishes usually moved to another from it.Territorial fishes such as T.moorei place and watched for other chances of attack- and Petrochromis spp.most severely chased it. ing.

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Table 5.Stomach contents of Perissodus microlepis.f,frequency of occurrence in percent; n,mean number;m,maximum number.

The number of attacks which one individual often saw the young make oral contact with the of prey fish suffered was not observed in this surface of their parents' bodies.This behaviour study,but Mr.K.Yamaoka recorded it in some has already been reported in some other cichlids algae-eating cichlids in the Luhanga quadrat and it has been considered that the young ob- in 1980 and 1981(unpublished data),while tain the mucus from the parents(Noakes and observing their feeding behaviour(Yamaoka, Barlow,1973;Noakes,1979).This behaviour 1982,1983).Petrochromis fasciatus was attacked of P.microlepis also may have a trophic function, once in 564 min observation but P.polyodon though we could not detect mucus-like materials and T.moorei were never attacked in 975 and in the stomach contents. 260 min observations,respectively.This sug- The juveniles less than 60 mm SL,some of gests that each individual of prey fish suffers which are schooling and others solitary,take little from the attack of P.microlepis. a wide variety of items.They feed on phyto- Stomach contents.The young guarded by plankters,zooplankters,benthic animals and the parents(see Yanagisawa and Nshombo scales(Table 5).Unidentified filamentous (1983)for their behaviour)mainly feed on materials were also abundantly found in their copepods,copepod nauplii and other zooplank- stomachs.Most of the phytoplankters were ters(Table 5).Scales never occurred in their the green algae Anabaena flosaquare,whose dense stomachs.The presence of sand in their stomachs surface accumulations were observed in October indicates that they also pick up materials from 1981.At the northern end of the lake,a bloom the substrate.In underwater observations,we of this algae occurs in September and October

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Table 6.Relationship between standard length of Perissodus microlepis and diameter of scales in its stomach.Two-hundred scales were measured for each size-class.

every year(Dubois,1958;Hecky et al.,1981). serve for this purpose.Since prey either Copepods,nauplii and ostracods eaten by counterattacks the predator or escapes from it if juveniles were fewer than those eaten by the they can notice its approach beforehand,these young guarded by the parents.About a half of tactics may be prerequisite for successful attack- the juveniles were taking scales,but the number ing. of scales in one stomach was much smaller than P.microlepis removed scales from many fish that of scales eaten by an adult. species.But its preference for fishes larger than, Scales were almost always found in the or as large as,itself and for those with deep stomachs of adults more than 60mm SL(Table body shape are obvious(Table 3).The pref- 5).The maximum number in one stomach was erence for the former is common to the majority 867.Scales in a stomach are tightly piled up of scale-eating fishes(Fryer and Iles,1972; like a pack of cards.They become thin and Major,1973;Sazima,1983)and the preference soft in the posterior part of the stomach and are for the latter is indicated in Therapon jarbua converted into a white paste at the end of the (Whitfield and Blaber,1978).A large target intestine,indicating that they are digested.The area such prey provide may be a primary reason mean diameter of scales in a stomach increases for these preferences.Frequent attacks on as the body size of the fish increases(Table 6). algae-eaters,such as Tropheus moorei,Petro- About 20 percent of adults examined were chromis spp.and Simochromis spp.,may be in taking some zooplankters,but copepod nauplii part due to their feeding activity on the open were never found.Fish larvae,probably of rock surface(see Yamaoka,1982)other than Lamprichthys tanganicanus,were found in 4 the above features.This contrasts with very adults. rare attacks on the carnivores Lamprologus Caloric value of scales.Caloric values of furcifer,L.leleupi and scales from P.polyodon,T.moorei and C.fur- which remain close to the more or less sheltered cifer were 2,210,1,779 and 2,250 cal g• dry wt-1. rock substrate. The average was 2,080 cal g• dry wt Juvenile P.microlepis take a wide variety of food items besides scales but the adults mainly Discussion feed on scales.Such change in diet with growth Brichard(1978)mentioned that P.microlepis is also known in the characoid scale-eater was seen"always in mid-water and not near the Roeboides(Roberts,1970;Sazima,1983).The rock shore".Certainly,this fish spends much majority of adult P.microlepis,however,take of its time in the water column.However,we other food at the same time.In one case,more observed that it came down to the substrate very than a thousand copepods occurred in a stomach often and three quarters of attacks on prey fishes (Table 5).Parents guarding young were seem- were made from the substrate.To come in ingly more dependent on zooplankters than were contact with the substrate is obviously one solitary adults,owing to the limitation of their tactics for approaching prey without being movements,though not quantitatively ascer- noticed.For this purpose it exploits additional tained yet.P.microlepis is a specialized scale- tactics;it ambushed using the shady sides of eater but is still euryphagous,as are most of rocks as cover and selectively directed its attacks the other lepidophagous fishes(Roberts,1970; to fishes engaging in feeding or social activity. Zaret and Rand,1971;Sazima,1977,1983). Fading its body stripes before attacking may also The caloric value of scales measured in the

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present study(=2 cal• mg -1)is nearly equal to 56041032,57043028,48041043,59043039)and that from other fish(Whitfield and Blaber,1978). for the Special Project Research(Nos.58121004, Mucus covering the scales is said to be rich in 59115004)from the Ministry of Education, protein and lipids(Wessler and Werner,1957; Science and Culture,Japan. Lewis,1970).Here we tentatively compare feeding efficiency between scale-eating and Literature cited feeding on zooplankters.An area of prey's Brichard, P. 1978. Fishes of Lake Tanganyika. scales dislodged by an attack of P.microlepis is T. F. H. Publ., Neptune City, 448 pp. estimated to be 50mm2,which was calculated Dubois, T. 1958. Evolution de la temperature, de from the area covered by teeth-marks when the l'oxygene dissous et de la transparence dans la mouth of adult was fully open.This value is baie nord du Lac Tanganyika. Hydrobiologia, equivalent to 6 mg,when measured in Tropheus 10 : 215-240. Fryer, G. 1959. The trophic interrelationships and moorei and Cyathopharynx furcifer.Therefore, ecology of some littoral communities of Lake the caloric value of scales obtained by one Nyasa with special reference to the fishes, and a attack is about 12 cal.On the other hand,one discussion of the evolution of a group of rock- zooplankter contains about 0.03 cal,provided frequenting Cichlidae. Proc. Zool. Soc. Lond., its caloric value being 5.5 cal• mg-1 and the 132 : 153-281. mean weight of one individual being 0.005mg Fryer, G. and T. D. Iles. 1972. The cichlid fishes of (an estimation from a common copepod Meso- the Great Lakes of Africa. Oliver and Boyd, cyclops leuckarti).Accordingly,scales obtained Edinburgh, 641 pp. by one attack correspond to some 400 zoo- Greenwood, P. H. 1964. Explosive speciation in African lakes. Proc. Roy. Inst., 40 : 256-269. plankters in calorie.For the planktivore Lamprologus brichardi inhabiting the same area Hecky, R. E., E. J. Fee, H. J. Kling and J. W. M. Rudd. 1981. Relationship between primary pro- as P.microlepis,it took 5.8 min on average to duction and fish production in Lake Tanganyika. pick up 400 plankters during the daytime 0800 Trans. Amer. Fish. Soc., 110 : 336-345. and 1600(Gashagaza,unpublished data).This Hori, M. 1983. Feeding ecology of thirteen species value is not much different from the time re- of Lamprologus (Teleostei; Cichlidae) coexisting at quired for one successful attack by P.microlepis a rocky shore of Lake Tanganyika. Physiol. observed in this study(=3.75 min).This sug- Ecol. Japan, 20 : 129-149. gests that scale-eating has a comparable feeding Hori, M., K. Yamaoka, K. Takamura, 1983. Abund- efficiency to feeding on zooplankters. ance and micro-distribution of cichlid fishes on a Scales are easily renewable through regenera- rocky shore of Lake Tanganyika. African Study tion(Sazima,1983).So,scales may be one of Monogr., 3 : 25-38. Lewis, R. W. 1970. Fish cutaneous mucus : a new the most stable food resources in the habitats source of skin surface lipids. Lipids, 5 : 947-949. where many fishes inhabit together.The Liem, K. F. and D. J. Stewart. 1976. Evolution of parallel adoptions of scale-eating habit in a the scale-eating cichlid fishes of Lake Tanganyika : number of fish species in both freshwater and a generic revision with a description of a new the sea(see Sazima,1983)may be attributed species. Bull. Mus. Comp. Zool., 147 : 319-350. to this feature. Major, P. F. 1973. Scale-feeding behavior of the leatherjacket, Scomberoides lysan and two species Acknowledgments of the genus Oligoplites (Pisces : Carangidae). We wish to thank H.Kawanabe,E.Harada, Copeia, 1973 : 151-154. Noakes, D. L. G. 1979. Parent-touching behavior J.T.Moyer,T.Narita,M.Hori and K.Yamaoka by young fishes : incidence, function and causa- for their helpful discussions and valuable com- tion. Env. Biol. Fish., 4 : 389-400. ments on the manuscript.We also grateful to Noakes, D. L. G. and G. W. Barlow. 1973. Ontogeny M.K.Kwetuenda,S.Yamagishi,M.Nishida, of parent-contacting in young Cichlasoma citri- T.Kondo,N.B.Mbomba,M.M.Gashagaza, nellum (Pisces, Cichlidae). Behaviour, 46 : 221-255. N.K.Mihigo and N.Mulimbwa for their advice Poll, M. 1956. Poissons cichlidae. Exploration and assistance during the course of this work. Hydrobiologiqued du Lac Tanganika (1946-1947), This work is supported partly by the Grant-in- 3, Fasc. 5B : 1-619. Aid for Overseas Scientific Survey(Nos. Roberts, T. R. 1970. Scale-eating American

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characoid fishes, with special reference to Pro- exclusion principle. Ecology, 52 : 336-342. bolodus heterostomus. Proc. Calif. Acad. Sci., 38 : 383-390. (NM : Institut de Recherche Scientifique (I. R. S.)/ Sazima, I. 1977. Possible case of aggressive mimicry Uvira, Uvira, Zaire; YY: Department of Biology, in a neotropical scale-eating fish. Nature, 270 : Ehime University, Matsuyama 790, Japan; MN: 510-512. Faculty of Fisheries, University of Mie, Tsu 514, Sazima, I. 1983.Scale-eating in characoids and other Japan) fishes. Env. Biol. Fish., 9 : 87-1011. Wessler, E. and I. Werner. 1957. On the chemical カ ワ ス ズ メ 科 魚 類Per'ssodus mimhpisの 「ウ ロ コ 食 composition of some mucous substances of fish. い 」 の 習 性 と 成 長 に 伴 う 食 性 の 変 化 Acta Chem. Scand., 2 : 1240-1247. Whitfield, A, K. and S. J, M. Blaber. 1978. Scale- Muaerhwa Nshombo・ 柳 沢 康 信 ・名 越 誠 eating habits of the marine teleost Terapon jarbua タ ン ガ ニ イ カ 湖 に 生 息 す るPerissodus microlepisの (Forska. 1). J. Fish Biol., 12 : 61-70. 「ウ ロ コ 食 い」 の 行 動 を 自 然 状 態 で 観 察 し た.ま た, Yamaoka, K. 1982. Morphology and feeding be- 種 々 の 発 育 段 階 の 個 体 の 胃 内 容 物 を 調 査 し た.親 に よ haviour of five species of genus Petrochromis っ て 保 護 さ れ て い る 稚 魚 は 主 に 動 物 プ ラ ン ク ト ン を 摂 Teleostei, Cichlidae).Physiol.Ecol.Japan,19:( 餌 し,親 か ら 独 立 後 の 未 成 魚 は,他 魚 の ウ ロ コ の ほ か 57-75. に 動 物 ・植 物 プ ラ ン ク トン,底 生 動 物 を 摂 餌 し た.成 Yamaoka, K. 1983. Feeding behaviour and dental 魚 は,多 く の 魚 種(特 に,大 型 で 体 高 の 高 い 付 着 藻 類 morphology of algae scraping cichlids (Pisces : 食 魚)か ら は ぎ と っ た ウ ロ コ を 主 要 な 餌 と し て い た 。 Teleostei) in Lake Tanganyika. African Study ウ ロ コ を と る た め の 攻 撃 は 主 に 基 底 近 くか ら 行 わ れ, Monogr., 4: 77-89. 時 に は,岩 の 下 面 や く ぼ み で 待 ち 伏 せ た 。 近 く を 通 過 Yanagisawa, Y. and M. Nshombo. 1983. Repro- し た 魚 の ほ か に,摂 餌 。ナ ワ バ リ 行 動 ・求 愛 行 動 に か duction and parental care of the scale-eating cichlid ま け て い る 魚 を よ く襲 っ た. fish Perissodus microlepis in Lake Tanganyika. Physiol. Ecol. Japan, 20 : 23-31. (Nshombo:ザ イ ー ル 国 科 学 庁 ウ ビ ラ 支 所;柳 沢:790 Zaret, T. M. and A. S. Rand. 1971. Competition in 松 山 市 文 京 町2つ 愛 媛 大 学 理 学 部 生 物 学 科;名 越: tropical stream fishes : support for the competitive 514津 市 江 戸 橋2-80三 重 大 学 水 産 学 部)

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