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Studies on the Development of the Labial Teeth Row Structure in Rana Curtipes Jerdon Tadpoles PDF

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STUDIES ON THE DEVELOPMENT OF THE LABIAL TEETH ROW STRUCTURE IN RANA CURTIPESJERDONTADPOLES 1 JineshJames,ThomasT. Valamparampil2andOommenV. Oommen3 (With oneplate) Key words: Rana curtipes, development, metamorphosis, labial teeth, tadpoles Thedevelopmentofthe labial teethrowstructureofanurantadpolesofthetemperateregionshas been studied. However, similar studies on tropical species are scant. The present study is an attempt to describe the ontogeny ofthe labial teeth row structure ofRana curtipes an endemic , species ofthe Western Ghats ofIndia. R. curtipes tadpole has the highest reported number of labia! teeth rows, with marginal teeth, among tropical frogs. Introduction wereusedforthestudy.Freshlycollectedeggswere dividedintogroupsof50andtransferredtoalarge The teeth of frogs function primarily to aquarium(maintainedataphotoperiodof12L:12D graspprey,ortopositionitforswallowing.Their at 29 ±2 °C) containing fresh pond water. After distributionisknowntobevariableevenamong hatching,thetadpolesweredividedintogroupsof closely related groups (Altig 1970). The oral 10 to avoid overcrowding, and reared in an armature ofthe larvae differs from that of the aquarium ofthe same size (Group A). Waterwas adults, as they differ in feeding habits. changedevery secondday, andthe tadpoles were The ontogeny of the labial teeth row fedadlibitumwithboiledspinach.Thedeveloping structure of anuran tadpoles inhabiting eggs and embryoswere observedunderbinocular temperate regions has been studied by several microscopetonotemorphological changes atone workers(Taylor 1942,Zweifel 1964,Altig 1970, hour intervals. Embryos and larvae were staged Lee 1976, Webb and Korky 1977, Hero 1990 according to Gosner (1960) system for Rana and Davies 1992). However, our knowledge of pipiens. Tadpolesofearlierstageswerepreserved theIndianamphibiansisscant.Rao(1914),Lobo in 5% and later in 10% formaldehyde. (1961), Chari (1962), Daniel (1975), Inger et Morphological features ofthe oral armature were al. (1984) and Sekar (1990a) have given brief studied,andtheteethrowformulawasdetermined notes on the mouth parts ofIndian amphibians. asperAltig(1970)modifiedbyWebbandKorky Agarwal and Niazi (1980), and Dutta and (1977),tointroducethe“marginalteeth”.Tadpole Mohanty-Hejmadi (1983) have reported the stages fromfeedingstage onwardswerecollected ontogeny of the teeth row structure in Rana from a natural habitat near Thekkady (76° 50 'E, tigerina (now Hoplobatrachus tigerinus). The 9° 45 'N), Kerala (Group B). Twenty to thirty presentpaperdescribeschanges intheteethrow tadpoles were examined at each developmental structure of Rana curtipes tadpoles during stage. metamorphosis. Results MaterialandMethods The number of teeth rows changed with growth.Thetadpolescollectedfromswiftwaters Fertilizedeggscollectedfromnaturalhabitat (stream) had more teeth rows than those reared ‘AcceptedJuly,1999 in the aquarium. A list ofteeth row formulae of 3DepartmentofZoology,S.B.College, tadpoles rearedin the aquariumat29 ±2°C, and Changanacherry,Kerala686101 India. 3DepartmentofZoology, Univers,ityofKerala,Karyavattom, those collected from a stream, have been Thiruvananthapuram695581,Kerala,India. presented in Tables 1 and 2. JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 97(2), AUG. 2000 223 )))))))))) )))))))))) THELABIALTEETHROWSTRUCTUREIN RANACURTIPESJ£7?£>6W TADPOLES Table1 Hatching and external gill stage: The LABIALTEETHROWFORMULAOFRANACURTIPES TADPOLES stomodaeum, at the anterio-ventral region, was Stages GroupA GroupB a deep oval pit at the time of hatching. At the Rearedinaquarium Collectedfrom external gill stage, it consisted ofa pair ofoval, naturalhabitat black,non-serratedbeakswithoutlabialteethand (stream) papillae. However, small indistinctridges could Formula Percent Formula be seen on the lateral and ventral margins, foreshadowing the labial teeth and papillae. External gillstage Withoutteeth Notcollected Oneexternalgillcoveredstage:Tadpoles Oneexternalgill l/0/2(l) 53 Notcollected reached one gill covered stage with widened coveredstage l/0/3(l) 47 mouth, and a single row ofpapillae on the sides Operculum 1/0/20) 20 Notcollected ofthe upper and lowerjaws. The edges of the completestage 2(2)/0/2(l 53 lower jaw had a single row of papillae, the 2(2)/0/3(l) 27 anterior edge ofthe upperjaw lacked papillae. Feedingstage 3(3)/0/3(l) 59 3(3)/0/3(l) Thebeaksbecameweaklyserrated.Atthisstage, 3(3)/0/4(l 41 3(3)/0/4(l) 53% of the tadpoles reared in the aquarium at Prelimbstage 4(3-4)/0/4(l) 20 4(3-4)/0/4(l) 5(3-5)/0/4(l) 46 5(3-5)/0/4(l) 29±2°C, had ateethrow formulaofl/0/2(l)and 5(3-5)/0/5(l) 26 5(3-5)/1/5(1) 47%had l/0/3(1);withacombinedformulaof1/ 5(3-5)/0/6(l 8 6(3-6)/l/6(l) 0/2-3(l) (Table 2). There was only one uninter- Limbbudstage 5(3-5)/1/5(1 14 6(3-6)/l/6(l) rupted row in the upperjaw. The number varied 6(3-6)/0/6(l) 30 7(3-7)/2/6(l) 6(3-6)/l/6(l) 36 8(3-8)/3/7(l from 2 to 3 in the lowerjaw, the firstbeing inter- 7(3-7)/l/6(l) 20 8(3-8)/4/8(l) ruptedbyamedialgap.Marginalteethwereabsent. 9(3-9)/4/7(1 Operculumcompletestage: Atthisstage, 9(3-9)/4/8(l 20% of the tadpoles examined had l/0/2(l) Footpaddlestage 7(3-7)/2/6(l 27 8(3-8)/3/7(l) (Table 1), 53% had 2(2)/0/2(l), and 27% had 7(3-7)/2/7(l 34 8(3-8)/4/8(l 8(3-8)/3/6(l) 39 9(3-9)/5/7(l 2(2)/0/3(l) formulae. The firstrow in the upper, 9(3-9)/5/8(l) and the secondandthird in the lowerjaw, when 10(3-10)/5/8(l) present, were uninterrupted. However, the first Footstage 7(3-7)/2/7(1 22 8(3-8)/2/8(l row in the lower, and the second in the upper 8(3-8)/0/7(l) 56 9(3-9)/2/7(l) jaw, were centrally broken. In the majority of 8(3-8)/2/6(l) 22 9(3-9)/3/8(l) 9(3-9)/4/8(l) tadpoles, teeth in the two jaws were weakly 10(3-10)/3/8(l developed.Thecombinedteethrowformulawas Welldeveloped 7(2-7)/0/7(l) 36 8(3-8)/0/7(l) 1-2(2)70/2-3(1). hindlimbstage 8(3-8)/0/6(l 31 9(2-9)/0/8(l) Feeding stage: A single row of labial 8(2-8)/0/6(l) 33 9(3-9)/0/8(l) papillaeappearedaroundthelateralandposterior 10(2-10)/1/8(1) 10(3-10)/l/8(l) marginoftheanterio-ventralmouth. Thesecond Oneforelimbstage 7(1-7)/0/4(1 61 9(3-9)/0/6(1 continuousrowofteethintheupperjawappeared 8(2-8)/0/6(l) 39 8(2-8)/0/7(l) for the first time. The third and fourth rows of 7(1-7)/0/6(1 ventral jaw were poorly developed; marginal Bothlimband 5(1-5)/0/3(1-3) 8 5(1-5)/0/3(l-3) teeth were not present at this stage. The teeth tailstage 4(1-4)/0/3(l-3) 32 4(1-4)/0/2(1-2) row formula varied from 3(3)/0/3(l) to 3(3)/0/ 4(1-4)/0/2(l-2) 33 3(1-3)/0/3(1-3 3(1-3)/0/2(1-2 27 4(1), in two groups of tadpoles, and thus the combined formula 3(3)/0/3-4(l) was the same Frogletstage Withoutlabial Withoutlabial forboth groups. teeth teeth 224 JOURNAL, BOMBAYNATURAL HISTORYSOCIETY. 97(2), AUG. 2000 THELABIALTEETHROWSTRUCTUREIN RANACURTIPESJERDON TADPOLES James, Jinesh etal.: Rana curtipes Plate 1 Fig. 1: a. Mouth parts ofatadpoleofRana curtipes atfootpaddle stage (stage 34). b. Marginal teeth ofatadpole ofR. curtipes atfootpaddle stage (stage 34). LT-labial teeth, MT-marginal teeth. 226 JOURNAL, BOMBAY NATURAL HISTORY SOCIETY, 97(2), AUG. 2000 ) ) ) ))))) THELABIALTEETHROWSTRUCTUREIN RANACURTIPESJERDON TADPOLES Table 2 COMBINEDLABIALTEETHROWFORMULAOFRANACURTIPESTADPOLES Stages GroupA GroupB Generalcombined Rearedinaquarium Collectedfrom formula naturalhabitat(stream Externalgillstage Withoutteeth Notcollected Nil Oneexternalgillcoveredstage l/0/2-3(l) Notcollected l/0/2-3(l) Operculumcompletestage l-2(2)/0/2-3(l) Notcollected l-2(2)/0/2-3(l Feedingstage 3(3)/0/3-4(l) 3(3)/0/3-4(l) 3(3)/0/3-4(l) Prelimbstage 4-5(3-5)/0/4-6(l) 4-6(3-6)/0-l/4-6(l) 4-6(3-6)/0-l/4-6(l Limbbudstage 5-7(3-7)/0-1/5-60) 6-9(3-9)/l-4/6-8(l) 5-9(3-9)/0-4/5-8(1 Footpaddlestage 7-8(3-8)/2-3/6-70) 8-10(3-10)/3-5/7-8(l) 7-10(3-10)/2-5/6-8( 1 Footstage 7-8(3-8)/0-2/6-7(l 8-10(3-10)/2-4/7-8(l) 7-10(3-10)/0-4/6-8(l Welldevelopedbindlimbstage 7-8(2-8)/0/6-7(l) 8-10(2-10)/0-l/7-8(l) 7-10(2-10)/0-l/6-8(l Oneforelimbstage 7-8(1-8)/0/4-6(l) 7-9(1-9)/0/6-7(l) 7-9(1-9)/0/4-7(l) Bothlimbandtailstage 3-5(1-5)/0/2-3(1-3) 3-5(l-5)/0/2-3(l-3) 3-5(1-5)/0/2-3(l-3) Frogletstage Nil Nil Nil Prelimbstage: Theteethrowformulae of 7(3-7)/1/6(1) labial teeth row formulae. Group the tadpoles reared at 29 ±2 °C were 20% 4(3- B tadpoles varied widely in the number ofteeth 4)/0/4(l), 46% 5(3-5)/0/4(l), 26% 5(3-5)/0/5(l) rowsatthisstage(Table 1).Onerowofmarginal and 8% 5(3-5)/0/6(l). The lastrow ofthe lower teethappearedforthefirsttimeintadpolesreared jawin70%ofthetadpoleswaspoorlydeveloped. in the aquarium. Another characteristic was the The combined formula 4-5(3-5)/0/4-6(l) developmentoftwotothreerowsofsub-marginal indicated that, of4 to 5 rows in the upperjaw, papillaeonthesidesofbothjaws.Thelowerand the first two rows were uninterrupted, marginal upper beaks were strong, serrated and teeth were absent and in the lowerjaw the teeth keratinized. As in some ofthe previous stages, rows varied from 4 to 6, with the first row the last row oflabial teeth in the lowerjaw was uninterrupted.Tworowsofsubmarginalpapillae poorlydeveloped, orincomplete. The combined couldbeseenonthesidesoftheupperandlower teeth row formula was 5-7 (3-7)/0-l/5-6(l) in jaws. Group A and 6-9(3-9)/l-4/6-8(1) in Group B. The combined teeth row formula, 4-5 Foot paddle stage: The combined teeth (3-5)/0/4-6(l), of tadpoles reared in the lab rowformulaeofGroupA [7-8 (3-8)/2-3/6-7(1)] indicatesthepresenceofamaximumoffiverows and Group B [8-10(3-10)/3-5/7-8(1)] indicated in the upperjaw and six rows in the lowerjaw. that maximum upper labial, lower labial and The combined teeth row formula of tadpoles marginal teethappeared forthe firsttime in this collected from the stream was 4-6(3-6)/0-l/4- stage. Maximum upper labial teeth rows in 6(1). One row of marginal teeth was observed GroupA were 8 and in Group B10. Similarly, for the first time in 40% ofthe tadpoles. the maximum marginal teeth rows observed in Limb bud stage: In this stage of Group A were 3. In Group B, the minimum and development, Group A had 14% 5(3-5)/l/5(l), maximum marginal teeth rows were 3 and 5 30% 6(3-6)/0/6(l), 36% 6(3-6)/l/6(l) and 20% respectively (Plate 1). All the rows ofteeth in JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 97(2), AUG. 2000 227 THELABIALTEETHROWSTRUCTUREIN RANACURTIPESJERDON TADPOLES the upper and the lower jaws were well lateralsidesofmouthinthepreviousstages,were developed. absorbedandpapillaewereseeninsmallclusters Footstage: InGroupAtadpoles,22%had at the comers of the mouth. The homy beaks 7(3-7)/2/7(l), 56% had 8(3-8)/0/7(l) and the disappeared. The mouth widened, and the remaining 22% had 8(3-8)/2/6(l) formulae. comersreachedtheleveloftheposteriormargin Thus, 78% oftadpoles ofGroup A at this stage ofthe eyes. had 8 rows in the upperjaw. Another feature at this stage was the reduction in marginal teeth. Discussion 56% in Group A had completely lost their marginal teeth. Likewise, in Group B, the The present study shows that there are majority had less than 4 rows ofmarginal teeth. variations inthedevelopmentoflabialteethrow Acomparisonbetweenfootpaddleandfoot structureintropicalanurans.Thenumberofteeth stages indicates thatwhile there was an increase rowschangeswiththestageofdevelopment,and in the percentage oflabial teeth row number in for each stage there are individual variations. foot stage, a decrease in marginal teeth row Table 1 indicates that labial teeth appear at the numberalso occurredinbothgroups oftadpoles one external gill covered stage, and reach a full at the foot stage. complement of rows at the foot paddle stage. Well developed hindlimb stage: All the Labialteeth rowsmaintainthis full complement tadpoles ofGroup A and a number oftadpoles up tothewell-developedhindlimb stage. Before inGroupB hadlosttheirmarginal teeth. Second the onset of metamorphosis, labial teeth begin labial teeth row became broken in 69% of to shed and disappear with the completion of tadpoles. Thus, reduction or shedding oflabial metamorphosis. Dutta and Mohanty-Hejmadi teeth had started at this stage. None of the (1983)reportedasimilarpatterninRanatigerinci tadpoles hadthe full complementofteeth atthis (now Hoplobatrachus tigerinus). Further, the stage. present study shows that the teeth rows in the One forelimb stage: Teeth row formula upperjawvaryfrom 1 to 10. Similarly, thelabial varied from 7(1-7)/0/4(1) to 8(2-8)/0/6(l) in teethrows inthelowerjawvaryfrom2 to 8. The Group A tadpoles. The combined formula of combined teeth row formula for Rana curtipes Group B was 7-9(l-9)/0/6-7(l). In the majority according to Rao (1914) is 6-8(4-8)/6-8(l), and of tadpoles, both upper and lower jaw had Sekar (1990b) is 7(3-7)/5-8(l) or 7(4-7)/5-8(l). intermittently broken labial teeth rows. The The present observation agrees with the views sheddingoflabialteethhadalready startedprior of Rao (1914) and Sekar (1990b) in the to this stage. The rows ofsub-marginal papillae maximumnumberofrowsandnatureofthefirst were absorbed, and limited to the comers ofthe row inthe lowerjaw. mouth. The number ofpapillae decreased in the The present study established that Rana lower jaw. The horny beaks, both upper and curtipes tadpoles have marginal teeth, which lower, became thick, colourless orwhite, except make their first appearance in the prelimb stage atthe edges where they wereblack atthis stage. (Table 2), reach a maximum at the foot paddle Both limb and tail stage: In both groups stage, and begin to disappear at the foot stage. oftadpoles,thecombinedteethrowformulawas Thenumberofmarginal teethvaries from0 to 5 the same, 3-5(l-5)/0/2-3(l-3). All the rows in in Rana curtipes. Similar findings have been the upper and lowerjaws were interrupted with reported in R. pustulosa (Taylor 1942), R. lostteeth,andlimitedtothecomersofthemouth. tarahumarae(Zweifel 1955)andR. macroglossa The labial fringes, which were present on the (VolpeandHarvey 1958).Butnonehavereported 228 JOURNAL BOMBAYNATURAL HISTORYSOCIETY. 97(2). AUG. 2000 THELABIALTEETHROWSTRUCTUREIN RANACURTIPESJERDON TADPOLES thepresenceofmarginalteethinatropicalanuran. Indirana beddomii) [4(4)/0/4(1-2)] and Some differences were also found in the R. keralensis (now Limnonectes keralensis) number ofteeth rows between aquarium reared [2(2)/0/3], by Chari (1962) for R. malabarica tadpoles, and those collected from their natural [170/2(1)] andbySekar(1990b)forRhacophorus stream habitat. The tadpoles developed in the malabaricus [6(3-6)/0/3(1)], werelessthanthose aquariumdiffersignificantlyfromthosecollected of Rana curtipes. The maximum number from streams in the number, pattern and reported for R.tigerina (now Hoplobatrachus percentage ofoccurrence oflabial andmarginal tigerinus), by Dutta and Mohanty-Hejmadi teeth rows. In Rana curtipes 10 rows oflabial (1983), was 5(2-5)/0/(l-3). , teeth in the upper and 8 rows in lower jaw The above observations reveal that Rana indicate that the species has the largest number curtipes has the largest number of labial teeth oflabialteethrows amongtropical frogs. Labial rows among tropical anurans and the number teethrowformulaereportedbyIngeretal. (1984) ofteeth rows changes with the development of forR. temporalis [2(2)/0/2(1)],R. beddomi(now tadpoles. ReferENCES Agarwal, S.K. & I.A. Ntazi (1980): Development of theherpetofaunaofBelize.Herpetologica*32:211- mouthparts inthe tadpolesofRana tigerina Daud. 214. Proc. IndianAcad. Sci. (Anim.Sci.)89(2): 127-131. Lobo,L.(1961):Someobservationsonthemetamorphosis Altig,R.(1970):Akeytothetadpolesofthecontinental ofthe frog Rana curtipes Jerdon. Zoologica: New United StatesandCanada. Herpetologica26: 180- YorkZool.Soc. 46:10: 103-104. 207. Rao, C.R.N. (1914): LarvaofRana curtipes Boul. Rec. Chari, V.K. (1962): A description of the hitherto Ind. Mus. 10: 265-267. undescribed tadpole and some field notes on the Sekar,A.G.(1990a):Observationsonthedevelopmental fungoid frog,Ranamalabarica Bibron.J. Bombay stages of tadpoles of the Malabar gliding frog not. Hist. Soc. 59(1): 71-76. Rhacophorus malabaricus Jerdon, 1870 (Anura : Daniel, J.C. (1975): Field guide to the amphibians of Rhacophoridae). J. Bombay nat. Hist. Soc. 87(2): westernIndia.Part3.7.Bombaynat.Hist.Soc. 72(2): 223-226. 506-522. Sekar, A.G. (1990b): Notes on morphometry, ecology, Davies,M.(1992):EarlydevelopmentofLimnodynastes behaviour and food oftadpoles ofRana curtipes terraereginae and L. fletcheri (Anura : Jerdon 1853 .J. Bombaynat. Hist. Soc. 87(2):312- Leptodactylidae: Limnodynastinae). Trans.R.Soc. 313. S.Alist. 116(4): 117-122. Taylor,E.H.(1942): TadpolesofMexicananura. Univ. Dutta,S.K.&P. Mohanty-Hejmadi(1983):Ontogenyof KansasSci. Bull. 28: 37-55. teeth row structure in Rana tigerina tadpoles. Volpe, E.P. & S.M. Harvey (1958): Hybridization and J.Bombay, nat. Hist. Soc. 80: 517-528. larvaldevelopmentin RanapalmipesSpix.Copeia Gosner,K.L.(1960):Asimplifiedtableforstaginganuran 1958: 197-207. embryos and larvae with notes on identification. Webb,R.G.&J.K.Korky(1977):Variationintadpolesof Herpetologica16: 183-190. frogs ofthe Rana tarahumarae group in western Hero,J.M.(1990):Anillustratedkeytotadpolesoccurring Mexico (Anura : Ranidae). Herpetologica 33: 73- inthecentralAmazonrainforest,Manaus,Amazonas, 82. Brazil.AmazonianaXI(2):201-262. Zweifel,R.G.(1955):Ecology,distributionandsystematics Inger,R.F.,H.B.Shaffer,M.Koshy&R.Bak.de(1984): ofthe Rana boylei group. Univ. Calif. Publ. Zool. A reportonacollectionofamphibiansandreptiles 54:207-292. from the Ponmudi, Kerala,South India.J. Bombay Zweifel, R.G. (1964): Distribution and life history ofa nat. Hist. Soc. 81(2):406-427. central American frog, Rana vibicaria. Copeia Lee,J.C.(1976): RanamaculataBrocchi,anadditionto 1964(2):300-308. JOURNAL BOMBAYNATURAL HISTORYSOCIETY, 97(2). AUG. 2000 229

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