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On the Development of Some Bony Elements in the Ontogenesis of Five Species of Notothenioidei O

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On the Development of Some Bony Elements in the Ontogenesis of Five Species of Notothenioidei O Journal of Ichthyology, Vol. 44, No. 3, 2004, pp. 245–251. Translated from Voprosy Ikhtiologii, Vol. 44, No. 3, 2004, pp. 225–231. 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 Notothenioidei 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 245 246 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. (b–e, g–i) Transverse section of lower jaw, (f) frontal section of lower jaw, (b, c, e–i) 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 JOURNAL OF ICHTHYOLOGY Vol. 44 No. 3 2004 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.
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