Japanese Journal of Ichthyology 魚 類 学 雑 誌 Vol.31,No.4 1985 31巻4号1985年

Development of Median and Paired Fin Skeleton of Paralichthys olivaceus(Pleuronectiformes: )

Eduardo F.Balart (Received May 16,1984)

Abstract Development of median and paired fins and their supports are described for Paralichthys olivaceus,giving details on origin,shape,ossification and meristic counts.All fin supports begin to form through cartilage in the following sequence:pectoral(2.62mm SL),dorsal(4.60mm SL), caudal(5.55mm SL),anal(5.95mm SL) and pelvic fin support(8.57mm SL).Completion and partial ossification of fin structures are already present by the 40th day after hatching(ca.16mm SL),after eye migration.This study shows how developmental osteology may clarify identifica- tion and terminology of fish bones(e.g.,caudal skeleton).Comparisons with other species be- longing to Pleuronectiformes elucidate basic pattern of fin formation within the order,and depict interesting departures which may be of taxonomic and/or systematic utility.

Paralichthys olivaceus is one of the most ex- ranging from 38.90 to 107.15mm SL(locality ploited flounder in Japanese waters probably unknown),were kindly supplied by Dr.T. because its abundance close to shore.Actually Minami.Reared specimens were preserved in this species is also the subject of extensive either 5 % buffered formalin or Bouins solution, artificial propagation.Despite the increase in whilst wild specimens were fixed in 10 % formalin. fundamental knowledge about this flounder Clearing and staining were done by Dingerkus (e.g.,Okiyama,1967;Tsuruta and Omori,1976; and Uhler's(1977) method.However,speci- Minami,1982;Kuwahara and Suzuki,1982), mens fixed in Bouins were greately decalycified, information on osseous structure is scarce and and were therefore used only for cartilage ob- incomplete(Amaoka,1969),and as far as could servations.Since formalin even at as low a be determined only Okiyama's studies(1967; concentration as 5 % decalcifies bone,it may be 1974) contribute to knowledge on osteological presumed ossification took place a little before development.Studies on the osteological de- that stated in this work. velopment provides various information about Observations and drawings were made with a functional aspects of larval survival as well as Wild M5 and Nikon SMZ10 stereoscopic micro- providing a potential tool for taxonomic and scope with the aid of camera lucida.Measure- systematic works(Dunn,1983). ments of smaller specimens were made with a This paper deals with the development of Nikon V20 profile projector associated to a median and paired fins and their support of Nikon SMZ6F digital counter,and by a cali- Paralichthys olivaceus giving details on their brated ocular micrometer attached to a micro- origin,shape,ossification and meristic counts. scope.Larger specimens were measured with a Kanol dial caliper.Fin rays and pterygio- Materials and methods phores were counted regardless of their degree of A total of 164 specimens of Paralichthys development;counts on paired fins included olivaceus was used in this study.Of them,154 both sides. were laboratory-reared and ranged from 2.62 to Results 17.43mm in standard length(SL) 0-42 days after hatching(a.h.).Specimens were reared Caudal fin skeleton.The caudal fin complex at the Japan Sea Farming Association,Miyako (Fig.11) is integrated by 2 preural centra;a Station(Iwate Prefecture),and Kyoto Univer- detached autogenous parhypural;a broad ventral sity,Maizuru Fisheries Research Station(Kyoto hypural plate(H 1+2) articulated to 1st preural Prefecture).Fourteen wild-caught specimens centrum;a broad dorsal hypural plate(H 3+4)

―398― Balart:Development of Paralichthyid Skeleton

1.Development of caudal fin support in Paralichthys olivaceus.A,4 .87 mm SL;B,5.55 mm SL; C,6.98 mm SL;D,7.60 mm SL;E,8.31 mm SL;F,9 .37 mm SL;G,11.13mm SL;H,16.51mm SL;I,86.45mm SL.a,accesory cartilage;cp 1-2,preural centra 1-2;e,epural;h,hypural;n, notochord;ph,parhypural.Stippled areas show cartilage.Open areas show developing ossification except notochord.Scales indicate 1mm .

fused to the tip of 1st preural centrum;an notochord which probably correspond to 1st autogenous 5th hypural(H 5)having proximal and 2nd hypurals(Fig.1B).By 21 day a.h.the end very close to 2nd epural;2 epurals of con- parhypural is already detached from the noto- trasting size,being the anteriormost elongated chord(Fig.1C).Smaller specimens,i.e.,6.76 whilst the posterior epural is very reduced; mm SL,exhibits hypural 1 and 2 well fused to usually 13 branched rays supported by hypural each other as well as a small cartilage protruding pieces and 4 unbranched but segmented rays in posteriorly.Larger specimens,in contrast,have addition to an unsegmented spur raylet located a somewhat enlarged dorsal hypural plate and in both,dorsal and ventral sides.Total ray also develop neural and haemal arches belonging number,however,can range from 18 to 19 to the future preural centrum 2.By 24 day (Table 1)following 1+2+13+2+1 or 1+2 + a.h.(7.35-7.63 mm SL)2 cartilaginous epurals 13+1+1 caudal formula(dorsal spur+un- of nearly equal size appear.The dorsal hypural branched +branched+unbranched +ventral plate still remains incomplete.Among larger spur).Multiple and somewhat deep scissures specimens,i.e.7.60 mm SL,an early notochord are present on distal margin of parhypural and flexion is observed(Fig.1D),though it also hypural pieces.Developmental evidence assures occurs early in larger specimens(over 8 mm P.olivaceus lacks uroneurals as well as ural SL)belonging to younger batches(i.e.,20 days centra which are never observed. old).The notochord flexion is associated to its Caudal fin complex develops among 17 day own distal regression.Thus,by 9.37 mm SL old specimens(5.55-6.12 mm SL).Two small (25 days old)hypural 5 develops at the tip of cartilage buds appear ventral to the unflexed notochord(Fig.1F).The anteriormost epural

―399― 魚 類 学 雑 誌Japan.J.Ichthyol.31(4),1985

Fig.2.Development of anterior part of dorsal fin support in Paralichthys olivaceus.A,4.82mm SL; B,5.44mm SL;C,5.65mm SL;D,6.04mm SL;E,6.98mm SL;F,8.31mm SL;G,11.13mm SL;H,16.50mm SL;I,107.15mm SL.Dr,distal radial;Na,neural arch;Pr,proximal radial;Pp, anterior process;R,elongated ray.Stippled areas show cartilage.Open areas show developing ossification.Scales indicate 0.5mm.

looks already strikingly larger than the posterior and hypural plates develop later after metamor- one at this stage.By 30 days a.h.(9.55-12.08 phosis.A specimen 38.90mm SL has 3 shallow mm SL)preural centrum 1 ossifies like preceed- scissures in each central plate,whereas by 86.45 ing centra(Fig.1G).Hypural 5 looks like an mm SL they are multiple and deeper(Fig.1I). enlarged triangular cartilage.A notochord Caudal ray development is shown in Fig.7. remnant separates it from the epurals.The The rays appear prior to notochord flexion but hypural ossification is evident at 40 day a.h. unossified.The smallest specimen bearing rays (Fig.1H).This event seems to coincide with (3 rays)is 5.89mm SL(17 day old).Among the fusion of hypural plate 3+4 to preural 25 day old specimens(8.63-9.44mm SL)a full centrum 1,though the symphysial line is still complement of principal rays is present.Seg- apparent.The distal end of the hypurals and mentation is evident before 8.15mm SL and the anterior epural remain cartilaginous.Epural coincides with ray ossification.Ossification 2 looks very reduced and somewhat hidden by spreads out from mid-rays toward dorsal and the 1st epural.Hypural 5 inserts between the ventral rays.Branching of rays starts by 40 1st epural and the preceeding dorsal hypural days a.h.,that is,just after metamorphosis.A plate.Ossification of the cartilaginous caudal 16.12mm SL specimen has 9 branched rays support follows the formation pattern,that is, whilst by 17.43mm SL they totalled 11 in from the ventral hypural dorsad to the epurals. number.The ventral spur develops first,by Scissures on the distal margin of the parhypural 9.37mm SL,whereas the dorsal spur appears

―400― Balart:Development of Paralichthyid Skeleton

―401― 魚 類 学 雑 誌Japan.J.Ichthyol.31(4),1985

59-65 rays,whereas the dorsal fin exhibits 73- 85 pterygiophores associated to 74-86 rays (Table 1).Posterior rays are apically separated looking like branched rays.Their number is variable(Table 1).This species lacks spine-like rays as well as median radials. By 12 days a.h.the dorsal fin skeleton begins to form.The smallest specimen(4.60mm SL) shows 2 cartilaginous proximal radials,whereas other specimens have 2 or 3 in addition to a sole modified ray(Fig.2A).Distal radial cartilages appear by 14 days a.h.(over 4.75mm SL), the anteriormost being formed a little after the 2nd distal radial(Fig.2B,C).By 14-17 days a.h.the anterior process of 1st proximal radial is present in most specimens(Fig.2D). At this stage the dorsal fin support is located on the cranium behind the eyes.Subsequent de- velopment consists of formation of new ptery- Fig.3.Development of pterygiophore(above) giophores posteriad.During the postlarval stage and ray number(bottom)of dorsal fin in 5(rarely 6)elongated rays are observed anterior- Paralichthys olivaceus.DR,distal radial; ly,although all of them are still unossified. proximal.PR,radial. The pterygiophore number is described in rela- tion to fish length(Fig.3).The proximal by 9.55 mm SL. radial number increases suddenly by 20-21 days Dorsal and anal fin skeletons.Each soft ray a.h.,whereas that of the distal radials by 24-25 is articulated to a small distal radial as a simple days a.h.Afterward these numbers increase hinge whilst the distal radial is located between steadly by almost a full complement during the 2 elongated proximal radials(Fig.2).There is metamorphic period.Dorsal ray development not a ball and socket articulation between ptery- proceeds posteriad except for the anteriormost; giophores as found in most teleost fishes this 1st ray appears later and never becomes (Lindsey,1955),because the proximal radial elongated.It articulates directly to the anterior lacks a defined posterodorsal process.The an- process of 1st proximal radial.The dorsal ray teriormost dorsal proximal radial is enlarged number is depicted by Fig.3 in relation to fish and supports 3 rays:those posterior rays arti- length.Ossification begins at the anterior ptery- culate through corresponding distal radials giophores and seems to proceed posteriad.By whereas the 1st ray articulates directly to the 40 days a.h.(over 16 mm SL)ossification is well anterior process of 1st proximal radial.The established among proximal radials(Fig.2H) first anal proximal radial is modified into a but posteriorly.Distal radials partly ossify very large rod and supports 4 rays:the anteriormost late,over 100mm SL and never completely ray articulates directly to it,the 2nd ray through (Fig.2I).Dorsal rays,in contrast,ossify by a supernumerary distal radial,whereas the 2 30 days a.h.A 9.55 mm SL specimen exhibits posteriormost rays articulate by 2 common 6 anterior rays lightly ossified whereas by 11.13 distal radials.A reduced element which appears mm SL 61 rays were stained.Thus ossification later druing ontogeny is described under the seems to proceeds posteriad.Ossification of name of supernumerary distal radial.The first dorsal rays coincides with a shortening of the anal proximal radial,so-called the `abdominal anterior 5 elongated rays.Ray branching rod',closes the abdominal cavity posteriorly seems to be a very delayed process since it is together with the 1st haemal spine. observed among juveniles over 40mm SL.Ray The anal fin consists of 58-64 pterygiophores branching starts from posterior rays anteriad, plus a supernumerary distal radial associated to individuals being over 90mm SL when branch-

―402― Balart:Development of Paralichthyid Skeleton

A B

E

D C

F G H

Fig.4.Development of anterior part of anal fin support in Paralichthys olivaceus.A,6 .98 mm SL;B, 7.35 mm SL;C,8.31 mm SL;D,9.00 mm SL;E,9.37 mm SL;F,11.13 mm SL;G,17.43 mm SL; H,107.15 mm SL.a,anus;Ar,abdominal rod;Dr,distal radial;Ha,haemal arch;Pa,para- pophysis;Pr,proximal radial;Sdr,supernumerary distal radial.Stippled areas show cartilage. Open areas show developing ossification.Scales indicate 1 mm. ing becomes noticeable(Table 1). ing).By 20-21 days a.h.up to 27 distal radials Anal fin support begins to develop by 17 days are developing in specimens over 8.95 mm SL. a.h.,being an abdominal rod,the sole cartilag- The anteriormost distal radial corresponds to inous structure at this stage(Fig.4A).The the 2nd one of the juveniles.The first distal smallest specimen bearing it is 5.95 mm SL, radial or supernumerary distal radial forms by though the abdominal rod is consistently present 30-31 days a.h.(7.48-12.08 mm SL),usually over 6.32 mm SL.It is located below the 1st in specimens over 11 mm SL or already having haemal arch and vertically oriented behind the an almost full complement of proximal radials abdominal cavity.The pterygiophore number (Fig.4F).Like dorsal pterygiophores new ele- seems to be proportional to fish length(Fig.5). ments are added posteriad.Anal fin rays ap- Unlike the abdominal rod,the following prox- pear suddenly around 8 mm SL.It was not imal radials are very small(Figs.4B and follow- possible to detect the order of formation,though

•\ 403•\ 魚類学雑誌 Japan.J.Ichthyol.31(4),1985

the scapula and coracoid near mid-height. Characteristically the coracoid exhibits a pro- duced anterior process ventrally directed.Ra- dials differ in size as well in shape,the outer radial being the longest.Postcleithra are so firmly attached to each other that it is difficult to distinguish them as 2 structures at the first glance. Among the fins the pectoral fin is the first to develop although it is also the latest to become completely formed.The pectoral bud appears at hatching(2.62-2.85 mm SL).It consists of a rudimentary and cartilaginous coraco-scapula which promptly becomes articulated to the pectoral blade cartilage.The coraco-scapula becomes roughly triradiated or L-shaped(Fig. Fig.5.Development of pterygiophore(above) 6A)because the formation of a striking posterior and ray number(bottom)of anal fin in process is found on the coracoid portion by the Paralichthys olivaceus.Symbols like Fig.3. 3rd day a.h.(2.65-3.25 mm SL).At this stage a very thin dermal finfold is located outside the the anteriormost ray is clearly the last one to pectoral blade cartilage;they will become rays be formed.Ossification is first noticeable on and radials respectively.The cleithrum is barely the abdominal rod by 30 days a.h.at over a discernible and looks like a filament without size 9.50 mm SL(Fig.4F).Among 40 day old proper connection to the coraco-scapula cartilage specimens ossification is already settled in most (like Fig.6B)by 14 days a.h.(4.75-5.48 mm proximal radials(Fig.4G)but lacking in distal SL).However,the cleithrum ossifies later,by radials.Like the dorsal fin,anal distal radials 25 day a.h.as evidenced by alizarin uptaking ossify at over 100 mm SL.Central rays are the (Fig.6C).A conspicuous notch appears at the first to ossify,and then ossification spreads out anterior margin of the coraco-scapula which anteriorly and posteriorly.That process begins later,by border closing,becomes the scapula about 30 day a.h.(9.55-12.08 mm SL)and foramen(Figs.6C-E).The supracleithrum and almost finishes ten day later.Anal ray branch- the posttemporal are lightly ossified(Fig.6F) ing begins very late.In individuals at sizes by 30 day a.h.(9.55-12.08 mm SL).The upper over 90 mm SL branching becomes noticeable postcleithrum develops before the lower one (Table 1).The abdominal rod is always the also by 30 days a.h.in some specimens,though largest proximal radial.It meets the develop- larger specimens bear both slightly ossified ones ing 1st haemal spine thus closing the abdominal (Fig.6F).A small propterygium forms from cavity(Fig.4B).As development proceeds it the blade cartilage prior to complete detachment changes in shape from a vertical rod to a distinct of radial cartilages by 40-42 day a.h.(11.57- arc.The following 5 or 6 proximal radials are 17.43 mm SL).That small propterygium be- close to the abdominal rod,but never fuse to it, comes articulated to the innermost ray and at least on the surveyed fish. represents the 1st small cartilage of the outer Pectoral fin skeleton.The pectoral girdle series(Fig.6G).The coraco-scapula presents consists of posttemporal,supracleithrum,clei- two distinct centres of ossification which separate thrum,coracoid,scapula,2 postcleithra,4 them into two structures.The posterior radials and an outer series of small cartilages coracoid process enters into regression whilst associated to the pectoral rays.The ray count the anterior one becomes the same as the process ranges from 12 to 14,mostly 13(Table 1). of adult fishes,mainly during 30-40 days a.h. The posttemporal is somewhat modified by The pectoral rays experience a short period grooves and enclosed tubes associated to a where they are unossified and have the appear- sensory line branch.The cleithrum supports ance of dense fibrilose rods onto the dermal

•\ 404•\ Balart:Development of Paralichthyid Skeleton

B

A

C D E

G F H

Fig.6.Development of pectoral fin support in P.olivaceus.A,3.25 mm SL;B,5.58 mm SL;C,6.12 mm SL;D,8.31 mm SL;E,9.37 mm SL;F,11.10 mm SL;G,16.51 mm SL;H,38.90 mm SL. ap,anterior process;c,cleithrum;cs,coraco-scapula;or,outer cartilages;pc,postcleithra;pp, posterior process;pt,posttemporal;r,radial;s,supracleithrum.Stippled areas show cartilage. Open areas show developing ossification.Scales indicate 1 mm. finfold.Development of pectoral ray number the rays on the right side begin branching by is shown in Fig.7.The rays ossify at 40 days 53.10 mm SL.In the surveyed range branched at sizes over 16 mm SL.Ray branching begins ray number increases up to 8 rays on the left on the left side by 41.70 mm SL,when a sole side whereas 7 is the maximum number on the branched ray is present(Table 1).Conversely, right side.Except for this asymmetry no other

•\ 405•\ 魚類学雑誌 Japan.J.Ichthyol.31(4),1985

Fig.7.Development of ray number of pelvic(above),pectoral(middle)and caudal fin(bottom)in Paralichthys olivaceus.

significant difference is observed during the area sagitally flattened. flounder development,though there is a minor A lateral bud of connective tissue could be displacement of posttemporal attachment to observed in the belly prior to positive identifica- neurocranium. tion of the basipterygium through alcian blue Pelvic fin skeleton.The pelvic girdle consists treatment.The cartilaginous basipterygium is of basipterygium associated to 6 rays.The evident by 20-21 days a.h.in most specimens basipterygium is a compounding of an anterior over 7.30 mm SL.It is located behind the process like an elongated shaft,obliquely directed pectoral girdle.The anterior process looks into and hidden by the lower portion of the reduced and remains in a horizontal plane(Fig. cleithrum,which ends ventrally in an expanded 8A).Afterward this process grows into an

•\ 406•\ Balart:Development of Paralichthyid Skeleton

intercleithra space shaped like the typical basipterygium of this fish(Fig.8B—E).Three A B C small radial-like cartilaginous masses are re- corded by 40 days a.h.(over 16 mm SL),which probably become associated to ray bases,though later they are not recorded among juveniles.The ray occurs among larger 20 day old specimens, though they appear at minor lengths(i.e.,7.49 mm SL)within older specimens.Development and ossification of pelvic rays follow an inner- outer sequence.The ray number development is shown in Fig.7.Ossification begins by 30 E days a.h.(over 11 mm SL)in both,the basi- pterygium and rays(Fig.8D).Even at 40 days a.h.the lower part of the basipterygium still remains cartilaginous(Fig.8E).Branching of pelvic rays apparently start later after meta- morphosis.By 38.90 mm SL inner 4 rays of Fig.8.Development of pelvic fin support in both sides are already branched,and sub- Paralichthys olivaceus.A,7.35 mm SL;B, sequently branching reaches up to 5 in number 8.31 mm SL;C,9.37 mm SL;D,11.13 mm (Table 1)the smaller ray remaining unbranched. SL;E,16.51 mm SL.b,basipterygium; No significant differences are reported between m,metapterygium.Stippled areas show the blind and ocular side in this fin. cartilage.Open areas show developing os- sification.Scales indicate 0.25 mm. Discussion

At the onset of exogenous feeding,swimming their fig.2). abilities become fundamental for searching and Fusion of hypural pieces occurs early during capturing prey especially if we consider the high caudal development,so it is difficult to judge proportion of zooplankton in the diet of P. how many cartliage buds are really involucrated, olivaceus(Kuwahara and Suzuki,1982;Minami, especially on dorsal plate H 3+4.The actual 1982).However,locomotive structures differ dorsal plate currently represents 2 elements,but scarcely from that already present in the newly in fact I observed 3 to 4 primordial buds in P. hatched larvae,that is,median finfold,pectoral olivaceus,and Barrington(1937)described 4 fin bud and notochord.Prelarvae lack rigid buds in Pleuronectes platessa.Other authors mechanical support by which they apply stronger failed to note the compound nature of most action to the medium without suffering deforma- hypural plates because,either staining methods tion.The notochord offers limitations in this did not show cartilage details,or just because respect in spite of the advantage of its flexibility. hypural plates are really fused ab initio.The Other main restrictions lie in the maneuverability significance of this developmental trait remains and control of the body position.During the open to question.From this study it is clear postlarval stage,these limitations are partly that neither uroneurals,urodermals nor ural overcome by development of cartilaginous struc- centra are developed at all in P.olivaceus.Some tures like pterygiophores,hypurals,neural and authors consider the uroneural/urodermal as haemal arches,and dermal structures like fin fused to some other caudal structure(e.g., rays,vertebral centra and ribs.After metamor- Amaoka,1969;Kim,1973;Okiyama,1974),or phosis all locomotive structures are fully formed. interpret other elements with it(e.g.,Monod, The caudal complex of P.olivaceus resembles 1968;Amaoka,1969;Okiyama,1974)in spite that of American Paralichthys spp.described by of the fact that the structure has never been ob- Woolcott et al.(1968),though they made an served during ontogeny(Thompson and Cleve, erroneous interpretation of caudal structures 1936;Barrington,1937;Woolcot et al.,1968; and overlooked the 2nd epural(pictured in Futch et al.,1972;Hensley,1977;Futch,1977;

•\ 407•\ 魚類学雑誌 Japan.J.Ichthyol.31(4),1985

Sumida et al.,1979;Tucker,1982;present study) olivaceus(present author),whereas in Cithari- within Pleuronectiformes.Ural centra are only chthys spp.and Etropus spp.the ossification starts presumed by Hensley(1977)and Futch(1977) centrally spreading out anteriorly and posteriorly as being fused to the preural centrum 1(urostyle (Richardson and Joseph,1973;Tucker,1982), of most authors). As for anal rays all authors agree that the os- Hypural 5 remains distinct throughout de- sification begins from the central rays(Richardson velopment in P.olivaceus as well in representa- and Joseph,1973;Tucker,1982;present author). tives of the (Barrington,1937; Pterygiophores of both dorsal and anal fins are Thompson and Cleve,1936;Sumida et al., reported to begin the ossification from the an- 1979),and the (Futch et al.,1972). teriormost as shown in this study,and the same Conversely,the posteriormost epural,or the was stated by Hensley(1977)in Engyophrys unique epural according to the case,merges to senta. the upper hypural(H 5)in some bothid fishes The presence of an enlarged 1st dorsal and (Hensley,1977;Futch,1977),and the same is anal proximal radial is widely recorded among reported by Tucker(1982)within the Paralich- teleost fishes.This observation suggests an thyidae.An unfused condition may be regarded early fusion of at least 2 pieces,e.g.,Woolcot as primitive whilst a compound one as derived. et al.(1968)and Frame et al.(1978)within the Among the Pleuronectiformes formation and Pleuronectiformes.My findings in P.olivaceus, ossification of caudal fin support proceed from however,show the abdominal rod never derives the ventral side upward,whereas ossification of from 2 pieces,as seems to occur commonly in caudal rays begins near the central rays spread- the Perciformes(Kohno and Taki,1983),but ing out dorsally and ventrally.Only Tucker develops an expanded and complex distal head. (1982)describes ossification starting ventrally The same seems true concerning the anteriormost but soon also beginning from the dorsal end of dorsal proximal radial except for the Cynoglos- the fin support. sidae,where a broad cartilage plate occupies Some caudal characters considered of sys- the place of several anterior pterygiophores tematic value,such as presence or absence of (Ochiai,1966). uroneurals,lack proper support and consistence Elongated dorsal fin rays located anteriorly as evidenced here and in other developmental are frequently described during the early life works,whereas others should be considered, period in most families but Pleuronectidae and like the epural number or fusion of epural to Soleidae.When present,the anteriormost elon- hypural 5.Moreover,based on developmental gated ray usually corresponds to the 2nd ray evidence some features can be recognized as since the 1st ray develops later and never be- comes elongated.Their functional meaning is primitive or derived,and so bear potential utility for reassessment of systematic characters discussed by Moser(1981),whereas their system- within the Pleuronectiformes.Caudal termino- atic significance is pointed out by Okiyama logy should be based on developmental origin (1967)and Amaoka(1979). as much as possible,especially in this group Sequence of formation of pectoral fin support where fusion of tail structures is common. seems to be common to Pleuronectiformes as The pattern of formation of dorsal and anal well as most teleost fishes.All reports stated fin pterygiophores,that is,from anterior end pectoral rays developing after eye migration posteriad,seems to be general within the except for Chascanopsetta lugubris(Amaoka, Pleuronectiformes(Gutherz,1970;Futch et al., 1971),which can reach immense size prior to 1972;Hensley,1977;present author).Distal metamorphosis(i.e.,120 mm SL).The coracoid radial were observed to develop separated from develops 2 processes during ontogeny in P. and after serial proximal radial,so corroborat- olivaceus.The posterior process appears in all ing the view of Kohno and Taki(1983).The teleosts but remains somewhat developed mainly pattern of ossification differs though there are among lower teleosts,whilst the anterior process still few observations in this respect.Dorsal develops well mainly among higher teleost rays ossify from the anterior end posteriad in fishes.The cleithrum spination is not developed Cyclopsetta mbriata(Gutherz,1970)and P. in P.olivaceus as seems to be the rule among

•\ 408•\ Balart:Development of Paralichthyid Skeleton paralichthyid fishes(Amaoka,1979). psetta lugubris. Japan. J. Ichthylo., 18(1): 25- Asymmetry in this group is mainly in position 32, pl. 4. rather than in structure,concerning fins.How- Amaoka, K. 1979. Larvae and phylogeny of Pleuronectiformes (Psettodidae, Pleuronectidae, ever,Tucker(1982)reports differences in ossifica- Paralichthyidae, and ). Kaiyokagaku tion timing between paired fins,and Futch(1977) describes minor ray counts on the right side. (Marine Sciences), 11(2): 100-110. (In Japanese). Barrington, E. J. W. 1937. The structure and de- Other asymmetry,mainly of ray structure of the velopment of the tail in the plaice (Pleuronectes pectoral fin,is discussed with a wide material platessa) and the cod (Gadus morrhua). Quart. J. basis by Marsh(1977).As for P.olivaceus,a Micr. Sci., n. s., 79(315): 447-469. clear trend to fin ray simplification is evident on Dingerkus, G. and L. D. Uhler. 1977. Enzime the blind side within the surveyed range.Marsh clearing of alcian blue stained whole small ver- (1977),however,points out only segmented tebrates for demonstration of cartilage. Stain foreshortening but not fin ray simplification in Technol., 52(4): 229-232. the same species. Dunn, J. R. 1983. The utility of developmental Sequentially the pelvic fin seems to be the osteology in taxonomic and systematic studies of teleost larvae : a review. NOAA Technical Report latest to start formation in Pleuronectiformes NMFS Circular 450 : 1-19. (Okiyama,1974;Hensley,1977;Futch,1977; Frame, D. V., T. J. Andrewa and C. F. Cole. 1978. Sumida et al.,1979;Tucker,1982;Minami, Osteology of the American plaice, Hippoglossoides 1982;present author),as well in most teleosts. platessoides. Postilla (193): 1-32. However,completion of this fin occurs,charac- Futch, C. R. 1977. Larvae of Trichopsetta ventralis teristically,prior to pectoral completion in the (Pisces: Bothidae), with comments on intergeneric group,whereas the opposite statement is usual relationships within the Bothidae. Bull. Mar. among the Perciformes.Spination on the Sci., 27(4): 740-757. Futch, C. R., R. W. Topp and E. D. Houde. 1972. basipterygium is absent in P.olivaceus like in Developmental osteology of the lined sole, Achirus all reported paralichthyid fishes,in contrast to lineatus (Pisces : Soleidae). Contr. Mar. Sci., 16: bothid species(Amaoka,1979). 33-58. Gutherz, E. J. 1970. Characteristics of some larval Acknowledgments bothid , and development and distribu- I wish to express my gratitude to Prof.Tamo- tion of larval spotfin flounder, Cyclopsetta fim- tsu Iwai,Kyoto University,for his valuable briata (Bothidae). Fish. Bull., 68(2): 261-283. Hensley, D. A. 1977. Larval development of advice and continual encouragement throughout Engyophrys senta (Bothidae), with comments on this study,and criticism of the manuscript.I intermuscular bones in flatfishes. Bull. Mar. Sci., am grateful to Assoc.Prof.Masaru Tanaka 27(4): 681-703. Kyoto University,and Dr.Takashi Minami, Kim, Y. U. 1973. Comparative osteology of the Japan Sea Regional Fisheries Research La- right-eye flounders, subfamily Pleuronectinae boratory at Niigata,for generously supplying me fishes. Publ. Mar. Lab. Pusan Fish. Coll., 6: with laboratory reared material and their useful 1-38. (In Korean with English summary). comments.I am also indebted to Dr.Masa- Kohno, H. and Y. Taki. 1983. Comments on the nobu Matsuoka,Kyoto University,for kindly development of fin supports in fishes. Japan. J. translating Japanese articles,translating the Ichthyol., 30(3): 284-290. Kuwahara, A. and S. Suzuki. 1982. Vertical dis- present abstract into Japanese,his hearty en- tribution and feeding of a flounder Paralichthys couragement during the preparation of this olivaceus larva. Bull. Japan. Soc. Sci. Fish., study,and critical reading of the manuscript. 48(10): 1375-1381. (In Japanese with English summary). Literature cited Lindsey, C. C. 1955. Evolution of meristic relation Amaoka, K. 1969. Studies on the sinistral flounders in the dorsal and anal fins of teleost fishes. Trans. found in the waters around Japan. , Roy. Soc. Can., 49 (ser. 3): 35-49. anatomy, and phylogeny. J. Shimonoseki Univ., Marsh, E. 1977. Structural modifications of the 18(2): 65-340. pectoral fin rays in the order Pleuronectiformes. Amaoka, K. 1971. Studies on the larvae and Copeia, 1977(3): 575-578. juveniles of the sinistral flounders-II. Chascano- Minami, T. 1982. The early life history of a flounder

•\ 409•\ 魚類学雑誌 Japan. J. Ichthyol. 31(4), 1985

Paralichthys olivaceus. Bull. Japan. Soc. Sci. history of the Pacific halibut. (2). Distribution and Fish., 48(11): 1581-1588. (In Japanese with English early life history. Inst. Fish. Comm. Rep. (9): summary). 1-184. Monod, T. 1968. Le complexe urophore des pois- Tsuruta, Y. and M. Omori. 1976. Morphological sons teleosteens. Mem. Inst. Fr. Afr. Noire, (8) : characters of the oral organs of several 1-705. species and their feeding behavior. Tohoku J. Moser, H. G. 1981. Morphological and functional Agr. Res., 27(2): 92-114. aspects of marine fish larvae, pp. 90-131. In Tucker, J. W., Jr. 1982. Larval development of R. Lasker, ed., Marine fish larvae; morphology, cornutus, C. gymorhinus, C. spilo- ecology, and relation to fisheries. Univ. Washing- pterus, and Etropus crossotus (Bothidae), with notes ton Press. on larval occurrence. Fish. Bull., 80(1): 35-73. Ochiai, A. 1966. Studies on the comparative mor- Woolcott, W. S., C. Beirne, and W. M. Hall. 1968. phology and ecology of Japanese soles. Bull. Descriptive and comparative osteology of the Misaki Mar. Biol. Inst. Kyoto Univ., (3): 1-97, young of three species of flounders, genus Para- pls. 1-2. (In Japanese). lichthys. Chesapeake Sci., 9(2): 109-120 Okiyama, M. 1967. Studies on the early life history of a flounder, Paralichthys olivaceus (Temminck (Department of Fisheries,Faculty of Agriculture, et Schlegel). I. Descriptions of postlarvae. Bull. Kyoto University,Sakyo-ku,Kyoto 606,Japan) Japan Sea Reg. Fish. Res. Lab., 17: 1-12. (In Japanese with English summary). ヒラメの鰭支持骨の発達 Okiyama, M. 1974. Studies on the early life history Eduardo F.Balart of a flounder, Paralichthys olivaceus (Temminck ヒ ラ メ の 対 鰭 お よ び 不 対 鰭 支 持 骨 の 発 達 過 程 を 記 載 et Schlegel). II. Descriptions of juveniles and the し,そ れ ら の 形 成 開 始,形,骨 化,計 数 形 質 に つ い て comparison with those related species. Bull. 詳 細 に 検 討 し た.す べ て の 鰭 支 持 骨 に お い て,胸 鰭 Japan Sea Reg. Fish. Res. Lab., 25: 39-61. (In (2.62mm SL),背 鰭(4.60mm SL),尾 鰭(5・55mm Japanese with English summary). SL),臀 鰭(5.95mm SL),腹 鰭(8.57mm SL)の 順 Richardson, S. L. and E. B. Joseph. 1973. Larvae 序 に 従 っ て,ま ず 軟 骨 が 形 成 さ れ た 。 眼 球 移 動 の 後, and young of western North Atlantic bothid ふ 化 後40日(約16mm SL)ま で に 鰭 構 造 は 完 成 flatfishes Etropus microstomus and Citharichthys し,部 分 的 に 骨 化 し た.本 研 究 は 骨 格 系 の 発 達 過 程 の arctifrons in the Chesapeake Bight. Fish. Bull., 観 察 が 魚 の 骨(た と え ば 尾 骨)の 同 定 や 用 語 法 を 明 ら 71(3): 735-767. か に す る 可 能 性 を 示 し て い る.ま た,カ レイ 目 に 属 す Sumida, B. Y., E. H. Ahlstrom, and H. G. Moser. る 他 魚 種 と 比 較 し た と こ ろ,本 目 魚 種 の 鰭 形 成 過 程 に 1979. Early development of seven flatfishes of は 基 本 的 なパ タ ー ン が あ り,こ れ は 分 類 学 的 あ る い は the eastern North Pacific with heavily pigmented 系 統 分 類 学 的 に 有 効 で あ る 可 能 性 を 示 唆 し て い る。 larvae (Pisces, Pleuronectiformes). Fish Bull., 77(1): 105-145. (606京 都市左京区北白川追分町 京都大学農学部 水 Thompson, W. F. and R. V. Cleve. 1936. Life 産学教室)

― 410―