Journal of Ichthyology, Vol. 44, No. 3, 2004, pp. 245Ð251. Translated from Voprosy Ikhtiologii, Vol. 44, No. 3, 2004, pp. 225Ð231. Original Russian Text Copyright © 2004 by Voskoboœnikova, Malashichev, Voronina. English Translation Copyright © 2004 by MAIK “Nauka /Interperiodica” (Russia).

On the Development of Some Bony Elements in the Ontogenesis of Five Species of O. S. Voskoboœnikova1, E. B. Malashichev2, and E. P. Voronina1 1 Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034 Russia 2 St. Petersburg State University, Universitetskaya nab., St. Petersburg, 199034 Russia Received February 11, 2003

Abstract—Development of the fine structure of the anguloarticulare, retroarticulare, quadratum, urostyle, and uroneurale of five species of Notothenioidei is investigated: Lindbergichthys nudifrons, L. microps, Nototheni- opsis larseni, Trematomus newnesi, and Pleuragramma antarcticum. The dual (integumentary and substituting) origin of the anguloarticulare and quadratum, subtituting origin of the retroarticulare, integumentary origin of the urostyle and uroneurale are revealed. In the formation of details of bones of complex origin the integumen- tary components play a greater role than the integumentary components. The data of histological investigations generally correspond to those obtained by alizarin staining. Development of the quadratum and urostyle in Notothenioidei revealed by alizarin staining and confirmed by histological investigation does not correspond to that in other bony fishes and may be considered synapomorphies of the suborder Notothenioidei supplying con- vincing proof of their monophyly.

There are few recent histological investigations of (SL 14 and 17 mm), L. mizops (SL 24, 27, 30, 34, and the development of the skeleton of higher bony fishes in 39 mm), Nototheniops larseni (SL 19 mm), Tremato- ontogenesis. Such investigations may explain the origin mus newnesi (SL 12 mm), and Pleragramma ant- of particular bony elements, relationships between var- arcticum (SL 12, 14, and 24 mm). All larvae were fixed ious recent fish groups, and the monophyly of a partic- with formalin. Embedding in paraffin and preparation ular group. Our study is aimed at histological investiga- of histological sections was done according standard tions of the development of particular bony elements in methods, staining was further done according to Van- five species of Notothenioidei, its comparison with the Gizon or with soluble hematoxylin (Sigma) according data on their development in other bony fishes (Haines, to Harris, with ethyl eosin and alcian blue. Microphoto- 1937; Nelson, 1973; Francillon, 1974; Schultze and graphs were taken using an installation for digital Arratia, 1989), and its comparison with the results of microphotography Ista-Video TesT (St. Petersburg). alizarin staining of the skeleton of the considered spe- Names of bones are used according to Harrington cies (Voskoboœnikova et al., 1994; Voskoboœnikova and (1955), Monod (1968), and Jollie (1986). SL is the Kellerman, 1997; Voskoboœnikova, 2001; etc.). Both standard body length. the bones of complex origin and the bones of simple In the section “Results” the development of ele- origin are investigated—angulo- and retroarticulare ments of the posterior region of the lower jaw (angulo- connected with the posterior end of Meckel’s cartilage, and retroarticulare), of suspensory apparatus (quadra- the quadratum, urostyle, and uroneurale. The bones of tum and quadratojugale), and of the caudal fin are the lower jaw were selected for the study as their fine described in the order of increasing size of fishes of dif- structure is important in systematics of higher taxa of ferent species. Figures 1 and 3 start with a schematic Teleostei (Nelson, 1973), the quadratum and urostyle as presentation of the position of the considered bony ele- their development studied by alizarin mounts of ments in the corresponding skeletal region of Notothe- Notothenioidei differs from that of these elements in nioidei. other bony fishes (Schultze and Arratia, 1989; Vosk- oboœnikova, 2001; Voskoboœnikova and Grechanov, 2002; Voskoboœnikova and Laius, 2003). RESULTS Anguloarticulare (Fig. 1a). Angulare (an integu- MATERIAL AND METHODS mental component of anguloarticulare) is at first observed in the larva of P. antarcticum SL 14 mm The study is based on larvae of five species of (Fig. 1b). This is a thin homogeneous plate situated lat- Notothenioidei collected in various years in the Scotia erally on the cartilage of the posterior end of Meckel’s Sea by V. Slyusarchik and off the Kerguelen Islands by cartilage and below a small rounded cartilage which is A.F. Pushkin: Lindbergichthys nudifrons (Loennberg) a capitulum of quadratum. On an anterior area of

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246 VOSKOBOŒNIKOVA et al.

mx (a) hm o mt p ms prmx ep q q sop dn aar ra sym pro io

cmk an cmk

ra dn

q (c) (d) an ar

ra cmk

(b) cmk aar(art) an cmk an cmk (f) aar(an) ra aar(an) (e) q(qju)

css cmk aar(ar) q

cmk spl (g) (h) aar(an) (i)

Fig. 1. Development of anguloarticulare and retriarticulare in the Notothenioidei. (a) Splanchnocranium of Lindbergichthys mizops SL 28 mm; (b) Pleragramma antarcticum SL 14 mm; (c, d) L. mizops SL 24 mm; (e) P. antarcticum SL 24 mm; (f) L. mizops SL 34 mm; (g, h, i) L. mizops SL 39 mm. (bÐe, gÐi) Transverse section of lower jaw, (f) frontal section of lower jaw, (b, c, eÐi) left side, (d) right side of the head. aar—anguloarticulare; an—angulare; cmk—cartilago meckele; css—seismosensory canal; dn—den- tale; ep—ectopterygoideum; hm—hyomandibulare; io—interoperculum; ms—mesopterygoideum; mt—metapterygoideum; mx— maxillare; o—operculum; p—palatinum; prmx—praemaxillare; q—quadratum; q (qju)—integumentary element of quadratum; ra—retroarticulare; sop—suboperculum; spl—spleniale; sym—symplecticum.

Meckel’s cartilage closer to the integumentary dentale, of Meckel’s cartilage. Anteriorly, it fits the notch no anlage of angulare is found. In larvae of L. nudifrons formed of the lower branch and the coronoid process of SL 17 mm and N. larseni SL 19 mm angulare covers the dentale. Posteriorly, it almost reaches the posterior from above downwards almost the whole outer surface edge of Meckel’s cartilage. All over its length this

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ON THE DEVELOPMENT OF SOME BONY ELEMENTS 247 homogeneous plate is uniformly thick. In the larva of (Fig. 1i). In this, the largest of the available larvae, SL P. antarcticum SL 18 mm angulare is less developed. It 39 mm there is no destruction of cartilaginous tissue of is situated in the central part of the lateral surface of the the posterior end of Meckel’s cartlage, which denotes posterior end of Meckel’s cartilage. Anteriorly, it does the transition to endochondral ossification. not reach the notch of the dentale. Posteriorly, it does Retroarticulare (Fig. 1a). In the larva of P. ant- not reach the posterior end of Meckel’s cartilage. In the arcticum SL 14 mm (Fig. 1b) a dark band, ossification larva of L. mizops SL 24 mm the angulare does not only of the retroarticulare, appears at the posterior end of cover the outer surface of Meckel’s cartilage along its Meckel’s cartilage making a margin at the very bottom entire length from the notch of the dentale (Fig. 1c) to of this part of the cartilage. In the larva of L. nudifrons the posterior edge but also becomes much wider than SL 17 mm a narrow ossification extends upwards and this cartilage in the anterior part, so that Meckel’s car- anteriorly under the perichondrium of Meckel’s carti- tilage is seen as a small round piece of cartilage adjoin- lage, over a third of its posterior end, from below. In the ing to the lower part of the angulare. The latter is repre- larva of P. antarcticum SL 18 mm the retroarticulare is sented as a rather thick homogeneous bony plate. Pos- present only along the lower edge of the posterior end teriorly, in the region of the coronoid process, the of Meckel’s cartilage not reaching its posterior end. In angulare fully covers from the outside the widened part N. larseni SL 19 mm the retroarticulare is not yet devel- of Meckel’s cartilage (Fig. 1d). In the larva of P. ant- oped. In the larva of L. mizops SL 24 mm the retroartic- arcticum SL 24 mm the angulare has grown from above ulare on sections starts as a small dark strip on the lower downwards along the outer surface of the posterior end edge of Meckel’s cartilage at the level of the anterior of Meckel’s cartilage. Anteriorly, it reaches the notch of end of the facette articulating with the quadratum. Pro- the dentale. Posteriorly, it reaches the posterior edge of ceeding to the posterior end of this articulation, the Meckel’s cartilage (Fig. 1e). It is still thin. In the larva bone becomes thicker and noticeably proliferates under of L. mizops SL 27 mm the angulare grows still thicker. the perichondrium, almost reaching laterally and medi- The Meckel’s cartilage in its anterior part and at its ally the upper edge of Meckel’s cartilage and separating articulation with the quadratum is a small oval contact- its outer surface from the angulare (Fig. 1d). The ret- ing the inner surface of the angulare. It is rather high in roarticulare in the larva of P. antarcticum SL 24 mm is the area of the coronary process and the angulare does still a small ossification of the lower edge of the poste- not reach its upper end. In the larva SL 34 mm the artic- rior end of Meckel’s cartilage (Fig. 1e). In the larva of ulare becomes visible as a small bone under the peri- L. microps SL 27 mm the retroarticulare grows thicker chondrium of the articulating surface of Meckel’s carti- and it fully comprises the posterior lower end of lage (Fig. 1f). It is not connected with the angulare, Meckel’s cartilage. In the larva SL 30 mm, at the area covering at this area the Meckel’s cartilage laterally. In of articulation with the quadratum, the retroarticulare the larva of L mizops SL 39 mm the articulare is already comprises only a small upper area of the cartilage well developed, its greatest thickness is noted in the neighboring the quadratum. area of the coronoid process where the Meckel’s carti- Quadratum (Fig. 1a). The integumentary element lage is fully covered with this bone (Fig. 1g). In the of this bone is first recorded in the larva of N. larseni SL anterior part of the articulating surface with the quadra- 19 mm (Fig. 2a). It was previously considered to be the tum, the articulare remains only on the upper surface of quadratojugale (Jollie, 1986; Voskoboœnikova et al., Meckel’s cartilage, while its lateral and lower surfaces 1994). This is a small rod-like bone situated at the lat- are covered by the retroarticulare. The angulare as an eral surface of the lower articulating process of the hyo- elongated and thick bony strip almost fully forms the mandibular cartilage, anteriorly approaching the poste- lateral surface of the posterior end of the lower jaw. On rior end of cartilaginous quadratum not starting its ossi- the upper surface of Meckel’s cartilage it fuses almost fication by this time. In the larva of L. mizops SL 24 mm along all its length with the articulare and forms at an the substituting bone is already well developed under articulating part a large and rather acute lateral promi- the perichondrium of the cartilaginous element of the nence. The latter is situated in close proximity to a sim- quadratum. The integumentary element of the quadra- ilar prominence of the quadratum (Fig. 1h). Both these tum is still situated on the lateral surface of the prominences essentially form the greatest part of the sympelcticum, just starting ossification, extends ante- articulating surface of the lower jaw and quadratum. riad under the quadratum and its anterior end over a There are rather large aggregations of small round cells small stretch fuses with perichondrial ossification of along the surface of these prominences. Along the the quadratum becoming its posterior process (Fig. 2b). lower outer edge of the angulare the canal of the seis- A similar situation is observed in larger larvae of this mosensory system with neuromasts is clearly seen. The species SL 27, 30, and 34 mm. In the largest available neuromasts are represented as a bud of closely arranged larva SL 39 mm the integumentary element of the elongated cylindrical cells on the bottom of the canal. quadratum participates, together with the angulare, in a At the level of the coronoid process, its walls are sup- significant part of the formation of articulating surfaces ported by small rod-like bones, splenialia, the upper of of the quadratum and lower jaw (Fig. 1h). Further on, which are already fused with the angulare completing towards the posterior end, it subdivides into three fac- the process of formation of the anguloarticulare ets. With the upper end of one of them it attaches to the

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248 VOSKOBOŒNIKOVA et al.

qju adm sym

q

q sym q

q(qju) q(qju) (a) (b) (c)

Fig. 2. Development of the quadratum on the Notothenioidei. (a) Nototheniopsis larseni SL 19 mm; (b) Linsbergcihthys mizops SL 24 mm; (c) L. mizops 39 mm. Frontal (a) and transverse (b, c) sections of the quardate and articulating cartilages from the left side of the head. adm—musculus adductor mandibulae; qju—quadratojugale. Designations of other bones as in Fig. 1. quadratum properly, with the inner lower facet it curves In all investigated larvae no trace of anlage and of sub- inside and supports the lower end of the symplecticum, sequent fusion of two or three ural centers is found. with the outer lower facet it supports muscular tissue of the m. adductor mandibulare (Fig. 2c). DISCUSSION Urostyle and uroneurale (Fig. 3a). In the larvae Our study revealed a complex origin of two of three T. newnesi SL 12 mm and L. nudifrons SL 14 mm no investigated bony elements of the skull of Notothenioi- bony elements are found in the skeleton of the caudal dei—anguloarticulare and quadratojugale. Formation fin. For the first time, the urostyle as a very thin bony of the anguloarticualre starts with the anlage of an strip along the upper surface and, in some sections, integumentary element of the angulare on the lateral along the lower and lateral surfaces of chorda is found surface of Meckel’s cartilage. Later, it proliferates ante- in the larva of P. antarcticum SL 14 mm (Fig. 3b). In the riad up to the anterior end of the notch of dentale and larva of L. nudifrons SL 17 mm the urostyle is a thin posteriad to the posterior end of the notch of the den- dark strip situated along the outer surface of about the tale, as well as upwards and downwards and fully upper third of the chorda (Fig. 3c). It has no cartilagi- closes the Meckel’s cartilage laterally. At later stages of nous precursors of any kind and is an integumentary the development of Notothenioidei, the angulare plays element. The nerve tube and cartilaginous epural plate a significant part in the formation of the articulating are well seen above it. Cartilaginous epuralia are situ- surface of the lower jaw with the quadratum and forms ated vertically under the chorda. The larvae of a lateral prominence. The latter comprises about two- L. mizops SL 24, 27, 30, and 34 mm are characterized thirds of the width of the articulating facette. Much by a more developed urostyle comprising the chords as later than the angulare a substituting element of the a thick ring (Fig. 3d) along a rather considerable dis- articulare appears on the upper surface of the articulat- tance from the second preural center to the proximal ing facette. Later, it proliferates in an anterior direction ends of the posterior hypuralia. The epuralia remain and surrounds the posterior end of the Meckel’s carti- cartilaginous in all larvae. Only at 34 mm the beginning lage and its coronoid process. Up to this time the medial of ossification of the first epuralia is noted. In the larvae surface of the angulare fuses with the lateral surface of SL 24 and 27 mm two posterior the epuralia do not the articulare producing a common element the angu- ossify, in the larvae SL 30 and 34 mm all hypuralia are loarticulare. Approximately, at the same time, thin ossified. In the larva SL 39 mm on the cross section of integumentary bones, splenialia, appear on the lateral the caudal region, two small integumentary bones surface of the angulare. They form the walls and roof of appear closing the nerve tube at the sides. They seem to the seismosensiory canal and rather soon fuse with the be uroneuralia (Fig. 3e). Relative size of the chords angulare. Generally, our data correspond to those of decreases in comparison with the chorda of smaller lar- Haines (1937) and Francillon (1974) on the origin of vae. Only one-fourth of the epurale undergoes ossifica- the anguloarticulare as a result of the fusion of anlages tion. The urostyle is a homogeneous structure not of bones of the integumentary and the origin by reaching posteriorly the posterior ends of the hypuralia. replacement in other representatives of bony fishes.

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ON THE DEVELOPMENT OF SOME BONY ELEMENTS 249

ure un h5 ur h4

h3 ch

h1 + 2

(a) ph (b) h

e e

e ur un

ur ch ch ch

ur h h h

(c) (d) (e)

Fig. 3. Development of the urostyle and uroneurale in the Notothenioidei. (a) Skeleton of the caudal fin if neglecta SL 32.5 mm; (b) plauragramma antarcticum SL 14 mm; (c) Lindbergichthys nudifrons SL 17 mm; (d) L. mizops SL 24 mm; (e) L.mis- ops SL 39 mm. (bÐe) transverse sections. e—epurale; ch—chorda; h—hypurale; ph—parhyopurale; un—uroneurale; ur—urostyle.

Nelson’s (1973) classification of the bony fishes into erly start. In this period the integumentary element pro- two groups is based on the fusion of the angulare with liferates forward and attains the lower edge of the one of the bony elements—either the retroarticulare or quadratum and then fuses with this bone. Further on, the articulare. Our study demonstrates that the Nototh- the integumentary element of the quadratum remains enioidei belong to most bony fishes in which the angu- rather well separated from the quadratum properly lare is fused with the articulare and the retroarticulare forming the posterior process of this bone. Anteriorly, remains a free element. it significantly grows and forms the bulk of the articu- Investigation of the fine structure of the quadratum lating capitulum of this bone. In addition, it takes an in ontogenesis of the Notothenioidei revealed that the active part in the attachment of the lower end of the integumentary element is the earliest, as in the case of symplecticum and in the support of muscular tissue of the anguloarticulare. Initially, it is situated on the lateral the m. adductor mandibulare. In the present case, as in surface of the lower process of the hyoid cartilage and the case of the anguloarticulare, the integumentary ele- is not connected with the quadrate cartilage. Later, the ment is formed earlier and participates much more perichondral ossification of the lower end of the quad- actively in the formation of various structures of the rate cartilage and the formation of the quadratum prop- bone than the substituting element.

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250 VOSKOBOŒNIKOVA et al.

A characteristic trait of development of the quadra- smaller larva may indicate the earlier development of tum in the Notothenioidei in comparison with other the skeleton of the caudal fin in P. antarcticum leading bony fishes (Jollie, 1975; Peters, 1981; Arratia and to the unique structure of the skeleton of the caudal fin Schultze, 1991; Cubbage and Mabee, 1996; Mabee and in this species in comparison with other representatives Trender, 1996; Koumoundouros et al., 2000; Vosk- of the suborder Notothenioidei (Totton, 1914; Balush- oboœnikova and Grechanov, 2002) is the much earlier kin, 1984; Andersen, 1984; Vioskoboœnikova, 2001). formation of the integumentary element in comparison The results of histological investigation of the urostyle with the substituting element. This important trait of development was previously found in investigations of correspond to the previous data of the total alizarin alizarin mounts in species of most families of the sub- staining of caudal fins of the larvae of the Notothenioi- order Notothenioidei, except Bovichtus angustifrons dei (Voskoboœnikova et al., 1994; Voskoboœnikova and from the most primitive family of Bovichthidae (Vosk- Kellerman, 1997; Voskoboœnikova, 2001). No cartilagi- oboœnikova and Bryus, 2001) and is now confirmed by nous precursors of the urostyle were noted and there- the data of histological investigation. We consider this fore it is considered to be an integumentary element. trait of development of all advanced families of the The urostyle appears and develops as a general ele- Notothenioidei as a synapomorphy, offering important ment, no anlages of two or three ural centers are found. proof of their monophyly. This character is important as No cartilaginous precursors of uroneuralia are found at present some authors dispute the monophyletic ori- either. They are formed as paired integumentary bones gin of the Notothenioidei (Hastings, 1993; Lecontre on the sides of the nerve tube at the latest stages of the et al., 1997; Bargelloni and Lecontre, 1998). This is caudal fin skeleton. The anlage of the urostyle in the caused by the description of diagnostic characters of Notothenioidei significantly differs from that in other the Notothenioidei—the presence of one pair of nos- trils, three radialia in the skeleton of the pectoral fin, bony fishes, in most of whom the ural center or several and floating posterior ribs, one by one or in a complex centers start their development as paired anlages on the in some representatives of other suborders of Blennioi- sides of the chorda (Voskoboœnikova and Grechanov, dei s. l. 2002) or arise immediately as a ring of bony tissue Two opposite viewpoints were expressed on the ori- around the chorda (Schultze and Arratia, 1989; Vosk- gin of the posterior process of the quadratum. The first oboœnikova and Laius, 2003). We consider the special one suggested by Jollie (1975, 1986) assumes that the way of development of the ural center as a synapomor- posterior process of the quadratum is a vestige of the phy of the Notothenioidei also confirming their mono- integumentary quadratojugale which occurs as an inde- phyly, similarly to the development of the quadratum. pendent element only in remote precursors of bony Schultze and Arratia (1989) believe, on the problem of fishes—paleoniscids. Other authors believe that the the origin of the uroneuralia, that these elements have posterior process of the quadratum in Teleostei is cartilaginous precursors in the bony fishes and so they always formed after the beginning of ossification of the are the substituting elements. As we did not find any posterior lower part of the quadratum, is characterized cartilaginous precursors of the uroneuralia in the by its membrane origin (Arratia and Schultze, 1991; Notothenioidei, we joined the opposite viewpoint sug- Cubbage and Mabee, 1996; Mabee and Trendler, 1996; gested by Monod (1968) on the integumentary origin of etc.) and has nothing in common with the quadratoju- gale of Sarcopterigii and ganoid fishes (Arratia and these bony elements. Schultze, 1991). Our data on the development of the Comparison of the results of investigation of the quadratum clearly indicate the integumentary origin of considered bony elements of the Notothenioidei its posterior process. The anlage of the latter is indepen- obtained by total alizarin and hematoxylin staining dent not only in relation to the bony quadratum but also demonstrated that the data of histological analysis con- to the quadrate cartilage as was shown by Jollie (1975) with reference to pike Esox. Its position in larger larvae firm the results obtained by total staining with alizarin. and juveniles of the Notothenioidei corresponds to that in larvae of Lepisosterus of ganoid fishes (Arratia and Schultze, 1991) and larvae of pike (Jollie, 1975) con- ACKNOWLEDGMENTS firming the viewpoint of Jollie on its homology with the quadratojugale. The authors are sincerely grateful to V.G. Borkh- vardt, St. Petersburg State University, for valuable Investigation of the skeleton of the caudal fin in the Notothenioidei indicates that development of the uro- advice in the process of investigation and for critical style starts on the upper surface of the chorda, as was reading of the manuscript. The study is supported by found in the larva of L. nudifrons SL 17 mm. Later, the the Federal Subprogram “Investigation of the Antarc- urostyle expands, comprises the chords laterally, and tic” (Project “Complex Investigation of the Antarctic closes on its lower surface. In the larva of P. antarcti- Biota”) and by grants of the Russian Foundation for cum SL 14 mm the beginning of this process was Basic Research no. 00-15-97794 “Petersburg Ichthyo- observed. The presence of a more advanced state in a logical School” and 03-04-49627.

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