Japanese Journal of Ichthyology 魚 類 学 雑 誌 Vol.l.25,No.11978 25巻1号1978年

Comparative Morphology and Interspecific Relationships of the Cyprinid

Yasuhiko Taki,Akari Katsuyama and Tousei Urushido (Received November 22,1977)

Abstract Interspecific relationships were investigated in 23 species of the cyprinid genus Puntius on the basis of the features of infraorbital bones ,pharyngeal bones and their teeth, lateral folds and barbels on the snout ,and color pattern.Six phyletic groups were recognized in these .In general,species belonging to the same group have overlapped or about equal geographic distributions.Between Southeast Asian and Indo-Ceylonese groups a more or less distinct gap is found in the degree of development of lateral folds and barbels . The results of this study indicate that Bleeker's(1863)division of Puntius into the subgenera Puntius,Barbodes and Capoeta is not acceptable from a phylogenetic viewpoint .

catalogue number(in the case of catalogued Introduction specimen)are given in order.

The genus Puntius Hamilton is the largest Southeast Asian species.P.altus(Gunther): in number of species of all cyprinid genera 25;41.5-105.0 mm;Thailand,Vietnam; in Asian tropics.Fishes of this genus occur IBRP 3112,3218,3283,6092,6485.P. throughout the region from Pakistan to schwanenfeldi(Bleeker):17;35.0•`163.0 southern China,inhabiting various types of mm;Thailand,Vietnam,Indonesia;IBRP fresh waters.The status of Puntius is ob- 3187,3197, 3282,6705.P.gonionotus scure;the delimitation and nomenclatural (Bleeker):14;70.0-182.5 mm;Laos,Thai- validity of the genus have remained unsettled land,Vietnam,Indonesia;IBRP 3180,3195,

(Hora and Mukerji,1934;Smith,1945;Hoede- 3234,3289.P.orphoides(Valenciennes): man,1958;Myers,1960), largely owing to 15; 66.0-122.0 mm; Laos,Thailand,Viet- the scantiness in the knowledge of its inter- nam;IBRP 3079,3182,3285,4376,6223 . and infrageneric relationships. P.tetrazona(Bleeker):24;23.5-47.0 mm;

The primary aim of this study is to in- Indonesia;IBRP 3184,6874.P. partipen- vestigate relationships among species of Puntius tazona Fowler:24;21.0-35.5 mm;Thai- on morphological bases,in order to provide land;IBRP 3068,3166,3261. P. pentazona data necessary for the assessment of evolu- (Boulenger): 11; 21.5-51.0 mm; Iodonesia; tionary lines within the genus.To this end, IBRP 3265. P. rhomboocellatus Koumans: internal and external characters were ex- 2; 27.5, 32.0 mm; Indonesia;IBRP 3190. amined on a total of 23 species. P.everetti(Boulenger):18;16.0-83.0 mm;

5 of 18,Indonesia;IBRP 6726,6754;13 Materials and methods of 18,aquarium-rised non-catalogued speci-

This study was based primarily on speci- mens.P.lateristriga(Valenciennes):15; mens collected from Southeast Asia and de- 11.0-66.0 mm;Indonesia;IBRP 6720,6768. posited in the Institute for Breeding Research, P.fasciatus (Bleeker):18;20.0-88.5 mm;

Tokyo University of Agriculture(abbrevia- 10 of 18,Indonesia;IBRP 3266,6618;8 tion for catalogue number,IBRP).It also of 18,aquarium-raised non-catalogued speci- dealt with specimens obtained from aquarium mens.P.binotatus(Valenciennes): 12; 49.0 suppliers in Tokyo and those raised in 82.5 mm;Vietnam,Malaysia;IBRP 6231,•` the laboratory.In the following list of 6736,6875.P.oligolepis(Bleeker):4;24.0 materials,number of specimens,their range •`32.0 mm;1 of 4,Indonesia;IBRP 6827;3 for standard length,collecting locality and of 4, non-catalogued specimens from an

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aquarium fish dealer.P.stigmatosomus anterior.Terms pertaining to pharyngeal

Smith:8;37.5-68.0 mm;Laos,Vietnam; bones and their teeth used in this study are

IBRP 3094,6231,6736.P.leiacanthus shown in Fig.2. (Bleeker).26;35.5,•`83.0 mm;Laos, Thai- Comparative observations land,Vietnam;IBRP 3038,3211,3235,

4772,5209,6353. Infraorbital bones.In all species under

Indian and Ceylonese species.All of the study the infraorbital series consists of a

following materials are non-catalogued speci- lacrimal,three infraorbitals,and a dermo-

mens obtained from aquarium fish dealers. sphenotic (Fig.1).The antorbital is missing.

P.chola(Hamilton):2;50.0,55.0 mm.P. The third and fourth infraorbitals are fused

arulius(Jerdon):3;53.0,-64.5 mm.P. together into a large bone bordering the bot- tom of the orbit.This fused element is filamentosus(Valenciennes): 2;34.5,85.0 mm.P.titteya Deraniyagala:3;16.0•`27.0 termed infraorbital 3+4.In P.conchonius,

mm.P.conchonius(Hamilton):9;41.0, P.cumingi,P.ticto and P.nigrofasciatus,the

•`62.5 mm.P.cumingi(Gunther):2;37.5, infraorbital 3+4 is much broader than other

44.0 mm.P.ticto (Hamilton):8;30.5•`49.0 infraorbital elements,with the outer margin mm.P.nigrofasciatus(Gunther):12;25.0 greatly elevated(Fig.1A).Whereas in the •` 43.0 mm. remaining species the bone is only as broad

Infraorbital bones were observed on alizarin- as the other infraorbitals(Fig.1B). stained transparent specimens.Identification Pharyngeal bones and their teeth.All of of the bones was based on Nelson(1969). the 23 species examined have three rows of Pharyngeal bones were removed from the pharyngeal teeth.In general,the first(outer) pharynx, stained with alizarin red,and then row has two slender teeth,the second(mid- cleaned.For cyprinid pharyngeal bones and dle)row three teeth slightly thicker than the their teeth, Chu's(1935)terminology has first-row teeth,and the main(third or inner) been employed by many authors.He used row four or five teeth,of which the third the terms'anterior'and'posterior'(e.g., and fourth teeth are large and broad.The anterior edentulous process, posterior angle) tooth formula for each species is shown in to indicate the positions of regions of the Table 1. bones.The pharyngeal bones of cyprinids, The number of teeth in the main row is however,are in reality more upright than stable in the 2,3,5-5,3,2 species.While in recumbent,and there are some cases where two of the 2,3,4-4,3,2 species,P.tetrazona this indication does not apply(e.g.,the and P. lateristriga,a fifth tooth is added to anterior angle is sometimes posterior to the the main row in some individuals.Of the posterior angle in actual position).We there- total of 23 specimens of P.tetrazona,two fore consider it proper to use'dorsal'in had 2,3,5-4,3,2 teeth,one 2,3,4-5,3,2,and place of posterior and'ventral'instead of one 2,3,5-5,3,2;of the 15 specimens of P.

Fig.1.Two different types of infraorbital bones in Puntius.A,P.comingi,37.5 mm SL;B,P. orphoides,66.0 mm SL.Scales indicate 1 mm. Abbreviations;D,dermosphenotic;L,lacrimal; 2•`5,infraorbitals 2-5.

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―3― 魚類学雑誌 Japan.J.Ichthyol.25(1),1978 lateristriga,one was 2,3,4-5,3,2,and another species.In the combination of the structural one 2,3,5-4,3,2.Variations in the number features of the pharyngeal bones and teeth, of teeth in the minor rows appear arbitrary six different types are recognized in the 23 and are observed in both the 2,3,4-4,3,2 species examined in this study(Fig.2). and 2,3,5-5,3,2 species but more frequently Characters of each type are briefly described in the former.The deviant formulae ob- as follows.Type A:pharyngeal bones very served are:1,3,4,-4,3,2 (P.tetrazona,1 broad and stout;dorsal limb broad, its tip specimen;P.fasciatus,1),2,3,4-4,3,1(P. truncate;ventral limb short;upper angle lateristriga,1),2,4,4-4,3,2(P.tetrazona,1; hardly recognizable;teeth congregated,thick, P.lateristriga,1),1,3,5-5,3,1(P.altus,1), swollen at apex.Type B:pharyngeal bones 2, 5,6-7,3,2(P.everetti,1),and 3,3,4-4,3,2 narrow; tip of dorsal limb pointed,some- (P.partipentazona,1). times slightly recurved in-and upward;up- In contrast to the inconstancy in tooth per angle conspicuous;teeth coarsely set, formula,the structure of the pharyngeal slender.Type C: pharyngeal bones stout, bones and their teeth are uninform within a broad;tip of dorsal limb truncate;upper

Fig.2.Fronto-dorsal aspects of left pharyngeal and its teeth in Puntius to show six different types of their structure.A,P.gonionotus, 115.0mm SL;B.P.tetrazona,36.5 mm SL;C.P.fasciatus, 88.5 mm SL;D,P.binotatus,56.0 mm SL;E,P.filamentosus,34.5 mm SL;E',P.conchonius, 50.5 mm SL.Scales indicate 2 mm.Abbreviations:DL,dorsal limb;UA,upper angle;VL, ventral limb;I-III,first,second and main rows of teeth;5,fifth tooth in the main row.

―4― Taki,Katsuyama and Urushido:Morphology and Relationships of Puntius angle more or less conspicuous;teeth ag- gregated,broad.Type D.pharyngeal bones rather broad;tip of dorsal limb blunt,greatly recurved in- and forward;no upper angle; teeth aggregated,moderate in size.Type E:pharyngeal bones broad;tip of dorsal limb pointed;upper angle unrecognizable; teeth congregated,moderate in size.Type E':pharyngeal bones and their teeth resemble those of the type E in shape and structure, but teeth more coarsely set(this type was Fig.3.Semidiagrammatic illustration to show represented by E'because of its similarity to the location and naming of black body the type E).Characters of the pharyngeal markings in Puntius.Abbreviations:AB, bones and their teeth of each species are anal-basal marking; CD,caudal marking; indicated in Table 1 by type. NC,nuchal marking;OB,orbital mark- ing;PA,postanal marking;PC,pectoral Lateral folds and barbels on snout.In marking;SA,supraanal marking;SD, some cyprinid species a lateral fold is devel- subdorsal marking. oped on each side of the snout.An example of its shape and position is illustrated in recognized in the 23 species.It is noted that Taki(1975).In the species of Puntius dealt these markings are often subject to age varia- with in this study,the lateral folds show tions,and some markings appear only during various degrees of development.They are certain stages of growth.The seven types well developed in P.conchonius,P.cumingi, of color pattern are characterized as follows. P.ticto and P.nigrofasciatus;vestigial in P. Type A:body plain or with a caudal blotch binotatus,P.oligolepis,P. stigmatosomus,P. which tends to fade with growth.Type B: leiacanthus,P.chola,P.arulius,P.filamentosus with cross bars in orbital,supra-anal and and P.titteya;totally absent in the remain- caudal positions.Type C:with cross bars or ing species. roundish blotches in pectoral,subdorsal, The number of barbels is also subject to supra-anal and caudal positions;an orbital interspecific variation.Barbels are missing marking may be present.Type D.with in P.conchonius,P.cumingi,P.ticto and P. pectoral,subdorsal,supra-anal,anal-basal, nigrofasciatus;one pair is present near the postanal and caudal spots or blotches;some tip of the rostrum in P.tetrazona,P.parti- of them may be indistinct or absent,or pentazona,P.stigmatosomus,P.leiacanthas, connected to each other.Type E:with a P.chola,P. arulius and P.filamentosus;one caudal spot similar in shape and position to pair near the tip of the rostrum and another that in type D.Type F:with cross bars or one pair near the mouth angle are present roundish blotches in nuchal,subdorsal,supra- in all other species. anal and caudal positions;a spot may be Color pattern.Many species of Puntius present on back at posterior end of dorsal fin possess black body markings,which are quite base and another one on each side below it various in size and shape.However,homo- in P.filamentosus.Type G:with pectoral, logies in the markings can be assessed by the postanal and caudal cross bars or roundish location of pigmentations in relation to body spots;orbital and subdorsal bars present in parts(Kortmulder,1972).In this study the adult P.nigrofasciatus and juvenile P. cumingi. black body markings are categorized accord- Species included in each type are shown in ing to their position into orbital,nuchal,pecto- Table 1. ral,subdorsal,supra-anal,anal-basal,postanal, Type C requires special mention.Of the and caudal markings. Locations of these five species contained in this type,P.penta- markings are shown in Fig. 3. zona,P.rhomboocellatus and P.everetti are In the combination of the body markings, characterized by having cross bars or roundish seven different types of color pattern are or elliptical blotches in both juvenile and

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Fig.4.Black body markings in three species of Puntius.A,P.everetti,subadult,59 .5 mm SL; B,P.lateristriga,subadult,52.0mmSL;C•`E,P.fasciatus.C,juvenile,20 .0mmSL,D,

juvenile,25.5 mm SL,E,adult,63.4 mm SL.Note the resemblance of D to A and B. adult.In P.everetti a narrow indistict the extra tooth."Such a tendency is not longitudinal streak is seen in some formalin- found in Puntius.The plasticity in the num- preserved specimens(Fig.4A).In contrast, ber of main-row teeth in P.tetrazona and adult P.lateristriga has a broad longitudinal P.lateristriga seem to indicate that there is stripe in addition to two cross bands(Fig.4B), in Puntius an evolutionary trend in the and adult P.fasciatus has a body marked number of main-row teeth toward the increase with several longitudinal stripes with no from four to five or otherwise toward the trace of cross bars(Fig.4E).In the juvenile decrease from five to four,and that such stage,however,these two species possess species as P.tetrazona and P.lateristriga only corss bars or small spots which cor- are undergoing the modification from one respond in position to the bars and spots in formula to another.Difference in the num- other members of the same group.Rearing ber of main-row teeth can be considered to experiments with these two species revealed be of rather little taxonomic significance in that the juvenile markings are destined to be Puntius when the above evolutionary trend is connected with each other to form a longi- taken into consideration. tudinal stripe in the posteior half of the body The variations in minor-row tooth counts in adult P.lateristriga and several rows of are more arbitrary,involving both addition longitudinal stripes along the entire length to and subtraction from the basic numbers. of the body in adult P.fasciatus.In the These variations seem to be resulted chiefly course of change in color pattern,P.fasciatus from disturbance in the process of tooth even passes through stages of everetti-and replacement,as indicated in some North lateristriga-like patterns(Figs.4C,D).These American cyprinids and catostomids by Evans facts suggest the existence of a more or less and Deubler(1955),Weisel(1967)and Eastman neotenous phenomenon in coloration among and Underhill(1973).It is generally known the species belonging to type C. that the pharyngeal teeth of cyprinids suc- Other characters.Caudal skeleton and pec- cessively shed and are replaced by new teeth toral and pelvic girdles were also examined produced in the surrounding mucosa.Failure in the 23 species.There was no significant of a replacement tooth to ankylose to the difference in these characters. pharyngeal hone will result in subtraction from the tooth formula,and that of an old Discussion tooth to shed as it is destined to be replaced Eastman and Underhill(1973)showed in will account for addition to the formula.It the pharyngeal teeth of some North American is noteworthy that the variability in the num- cyprinids that"••cwhen addition of a major ber of minor-row teeth was pronounced again row tooth has resulted in an asymmetrical in P.tetrazona and P.lateristriga.In these formula the left arch has always received two species the plasticity in the number of

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main-row teeth appears to accompany the shape of the infraorbital 3+4(Fig.1A). instability in the minor-row dentition. A more or less pronounced gap occurs in Comparison of the characters of the 23 the degree of development of barbels and species here examined indicates that they con- lateral folds between the eastern(Southeast stitute six groups each consisting of species Asian)and western(Indian and Ceylonese) sharing these morphological features almost assemblages of groups(Table 1).The binotatus- completely(Table 1).The six groups are group appears to afford a link between the called in this paper altus-group,tetrazona- two assemblages in the respects that it is group,pentazona - group,binotatus-group, intermediate between the two in these morpho- arulius-group,and conchonius-group. logical characters and has a range that extends In the pentazona-group,P.fasciatus differs from Southeast Asia through India southward from other members in the structure of the to Ceylon.However,it is difficult to con- pharyngeal bones.Nevertheless,its similarity sider such a group with specialized pharyngeal to other members in all other characters bones as the binotatus-group to be a direct seems sufficient to justify its assignment to transitional form linking the eastern and the pentazona-group.In the same manner, western groups.Between Southeast Asia the uniformity in major characters of the and South India there are the drainages of four species of the binotatus-group should the Salwin,Irrawaddy and Ganges Rivers, suffice their inclusion in the same group in where numerous species of Puntius occur. spite of the difference in the number of barbels. Examination of species inhabiting these rivers In Puntius the number of barbels may not be is required to elucidate more clearly the lines of overriding phylogenetic significance. of differentiation and dispersal of Puntius. The morphological similarity as seen among Bleeker(1863)divided the genus Puntius species in each group is sufficient to suggest into three subgenera,Puntius,Barbodes and that members of the same group are de- Capoeta,based solely on the number of barbels. cendants from a common direct ancestral Though this classification has been followed stock.The distributional pattern of each by some authors,this subdivision is not ac- group supports this view;except for the ceptable because of the limited phylogenetical binotatus-group,species belonging to the same significance of the number of barbels as in- group have overlapped or otherwise proxi- dicated in this study. mate geographic ranges(Table 1). The four species of the altus-group are in Acknowledgments complete agreement in the characters ex- We are very grateful to Dr.Sajiro Makino, amined,and similar in geographic ranges, member of the Japan Academy,for the which encompass mainland Southeast Asia critical reading of the manuscript and valu- and the Greater Sunda Islands.They are able suggestions,and to Dr.Norio Kondo, all large-sized fishes for Puntius.In contrast, Tokyo University of Agriculture,for his sup- the members of the tetrazona- and pentazona- port to our study of Asian freshwater fishes. groups are variable in pharyngeal tooth Messers.Akira Imaki,Arata Kawamoto and formula.The latter group is variable in Atsushi Suzuki,the Institute for Breeding color pattern,too.These two groups should Research,Tokyo University of Agriculture, be in the course of diversification.All are acknowledged for technical assistance. species belonging to the two groups are Literature cited small colorful fishes.The binotatus-group is Bleeker, P. 1863. Atlas ichthyologique de Indes peculiar,and specialized,in the structure of the pharyngeal bones(Fig.2D).Of the three Orientales Neerlandaises, III. 150 pp.,pls. CII•` CXLIV. species of the arulius-group,P.titteya is a Chu, Y. T. 1935. Comparative studies on the tiny species,while other two are medium- scales and on the pharyngeals and their teeth sized.The conchonius-group resembles the in Chinese cyprinids, with particular reference tetrazona-and pentazona-groups in color pat- to and evolution. Biol. Bull. St. tern,but it is peculiar,and uniform,in the John's Univ., Shanghai, 2:i•`x,1•`25, pls.

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1•`30. I•`XI, 1•`622, figs. 1•`107, pls. 1•`3. Eastman, J. T. and J. C. Underhill. 1973. Intra- Taki, Y. 1975. New species of the genus Sca- specific variation in the pharyngeal tooth for- phognathops, , from the Lao Mekong mulae of some cyprinid fishes. Copeia, 1973 system. Japan. J. Ichthyol., 21 (3): 129-136, (1): 45•`53. figs. 1-3. Evans, H. E. and E. E. Deubler, Jr. 1955. Pharyn- Weisel, G. F. 1967. The pharyngeal teeth of

geal tooth replacement in Semotilus atromacu- larval and juvenile suckers (Catostomus). Copeia, latus and Clinostomus elongatus, two species of 1967 (1): 50-54, figs. 1-5. cyprinid fishes. Copeia, 1955 (1): 31-41, figs. 1•`5. (YT and AK, Tokyo University of Fisheries, Hoedeman, J. J. 1958. Le statut du genre 4-5-7, Konan, Minato-ku, Tokyo 108; TU, The

Cuvier & Cloquet, 1816. Beaufortia, 6: 199•` Institute for Breeding Research, Tokyo University 201. of Agriculture, 2-4-28, Kamiyoga, Setagaya, Hora, S. L. and D. D. Mukerji. 1934. Notes on Tokyo 158, Japan) fishes in the Indian Museum. XXIII. On a collection of fish from S. Shan States, Burma. コ イ科Puntius属 魚類 の 比 較 形 態 と種 間 関 係 Rec. Indian Mus., 36: 353-370, figs. 1-3. 多 紀保 彦 ・勝 山 明 里 ・漆 戸 登 宇 世

Kortmulder, K. 1972. A comparative study in 熱 帯 ア ジ ア 産 の コ イ 科Puntius属 の23種 に つ い て 夢 colour patterns and behaviour in seven Asiatic 眼 下 骨,咽 頭 骨 と咽 頭 歯,吻 部 のlateral foldsと 口 Barbus species (Cyprinidae, Ostaryophysi, ひ げ お よ び 斑 紋 の 比 較 を お こ な っ た 。 そ の 結 果,こ れ Osteichthyes). Behaviour, suppl. 19: I•`XIII , ら の 魚 種 は6系 統 群 に 分 か れ る こ と が 判 明 し た.一 般 1-327, figs. 1•`2. に 同 一 群 に 属 す る 種 は,分 布 域 も 重 な り合 っ て い る か Myers, G. S. 1960. Preface to any future classi- あ る い は 近 接 し て い る 。 東 南 ア ジ ア に 分 布 す る群 と イ fication of the cyprinid fishes of the genus ン ド ・セ イ ロ ン の 群 と の 間 に は,lateral foldsと 口 ひ Barbus. Stanford Ichthyol. Bull., 7 (4): 212,•` げ の 発 達 程 度 に 比 較 的 明 瞭 な 差 異 が あ る 。Bleeker 215. (1863)はPuntius属 をPuntius,Barbodes,Capoeta Nelson, G. S. 1969. Infraorbital bones and their の3亜 属 に 分 類 し た が,本 研 究 の 結 果 か ら み る と,こ bearing on the phylogeny and geography of の 亜 属 分 類 は 支 持 し が た い 。 osteoglossomorph fishes. Am. Mus. Nov.,

(2394): 1•`37, figs. 1•`22. (多紀 ・勝 山:108東 京 都 港 区 港 南4-5-7東 京 水産 Smith, H. M. 1945. The fresh-water fishes of 大 学.漆 戸:158東 京 都 世 田谷 区 上 用 賀24-28東 Siam, or Thailand. Bull. U. S. Nat. Mus., 188: 京農 業大 学 育 種 学 研 究 所)

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