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Ontogeny of the Osteocranium in the African Catfish, Clarias

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Ontogeny of the Osteocranium in the African Catfish, Clarias JOURNAL OF MORPHOLOGY 235:183–237 (1998) Ontogeny of the Osteocranium in the African Catfish, Clarias gariepinus Burchell (1822) (Siluriformes: Clariidae): Ossification Sequence as a Response to Functional Demands DOMINIQUE ADRIAENS* AND WALTER VERRAES Institute of Zoology, University of Ghent, Ghent, Belgium ABSTRACT The ontogeny of the bony skull of the African catfish, Clarias gariepinus, is studied from initial ossification until a complete skull is formed. The ossification sequence in C. gariepinus seems to be related to the func- tional demands that arise in a developing larva. Early ossification of the opercular bone coincides with the initiation of opercular skin movements. Early ossifications involve several dentulous bones, formed shortly before the transition phase from endogenous to exogenous feeding. The enlarging bran- chiostegal membrane becomes supported by the gradual adding of branchio- stegal rays. Parasphenoid ossification may be related to protection of the brain during prey transport, whereas the several hyoid bones, including the parurohyal, are formed in relation to the increasing loads exerted onto the tendons of the sternohyoideus and consequently onto the hyoid bar. Overall skull reinforcement occurs almost simultaneously, with a whole set of perichon- dral bones arising especially at places of high mechanical load. The suspenso- rium becomes protected against dislocation in an anteroposterior direction through a ligamentous connection, which even becomes partially ossified, forming the sesamoid entopterygoid. Later, the cranial lateral-line system becomes enclosed by a set of gutters, which close, frequently becoming plate-like later in ontogeny. The brain also becomes covered dorsally. Addi- tional dentition (prevomeral tooth plates) formation seems to coincide with formation of the opercular four-bar system, as well as with the time the digestive system becomes completely functional. Eventually, unossified re- gions between the bones become closed off, fortifying and completely covering the skull. J. Morphol. 235:183–237, 1998. ௠ 1998 Wiley-Liss, Inc. The osteology of catfishes has been a basis hito, ’91; Teugels et al., ’91; Kobayakawa, for several studies, especially for taxonomy ’92; Chen and Lundberg, ’95; de Pinna and and phylogeny. In the present study, the Vari, ’95; Ferraris, ’96). Special attention taxonomy follows that of Fink and Fink (’96), has been paid to some clariid species (Nawar, in which the Siluriformes, or catfish, repre- ’54; Greenwood, ’56; Poll, ’57, ’77; Tilak, ’63c). sent the sister group of the Gymnotiformes, Much confusion concerning homologies is or knife-fish. Both are grouped within the being cleared up, as data from several stud- Siluriphysi, which together with the Char- ies and several catfish groups are put to- aciphysi and Cypriniphysi comprise the oto- gether (Fink and Fink, ’81, ’96; Arratia and physan group of the Ostariophysi. An exten- Gayet, ’95; Arratia and Huaquin, ’95). For a sive literature has been produced on the general review of bone nomenclatural syn- descriptive cranial osteology of siluriform onymies, we also refer to Harrington (’55). fish, mostly on adult forms (e.g., McMurrich, 1884; Bhimachar, ’33; Merriman, ’40; Hubbs and Miller, ’60; Tilak, ’61, ’63a,b, ’64, ’65a,b, Contract grant sponsor: Institute for Science and Technology ’67, ’71; Rastogi, ’63; Gauba, ’66; ’70; Taverne (D.A.); contract grant sponsor: National Funds for Scientific and Aloulou-Triki, ’74; Lundberg, ’75, ’82; Research (W.V.). *Correspondence to: Dominique Adriaens, University of Srinivasa Rao and Lakshmi, ’84; Vignes and Ghent, Zoological Institute, K.L. Ledeganckstraat 35, B-9000 Garcia, ’87; de Pinna, ’88; Howes and Fumi- Gent, Belgium. E-mail: [email protected] ௠ 1998 WILEY-LISS, INC. 184 D. ADRIAENS AND W. VERRAES The main purposes of the present work MATERIALS AND METHODS are, first, to describe the ontogeny of the Observations were made on 30 different cranial bones in order to observe the pres- ontogenetic stages of the African catfish Clar- ence or absence of cranial bones. Addition- ias gariepinus, originally described by ally, ontogenetic stages provide information Burchell (1822) and synonymized by Teugels concerning fusions or reductions of certain (’82). Specimens ranged from 4.1 mm SL skeletal elements, of which no trace can be (standard length) (51 day posthatching) to seen in adults. Further, we attempt to con- 174.5 mm SL (age unknown) (Table 1). Eggs sider the ontogeny of skeletal elements from a functional morphological point of view. Why were obtained from the Laboratory of Ecol- do certain bones develop at a certain mo- ogy and Aquaculture (Catholic University of ment, and why do some develop simulta- Leuven) and raised at a temperature of 25°C. neously while others do not? Such attempts Most juveniles (100 days posthatching) were (Weisel, ’67; Verraes, ’74, ’75, ’77; Verraes commercially raised and obtained from W. and Ismail, ’80; Hunt von Herbing et al., Fleure (Someren, The Netherlands). At dif- ’96b; Mabee and Trendler, 1996) can yield ferent time intervals, the developing larvae important information on the adaptations of were sedated in MS-222 and fixed in 4% structures present at a certain stage. Addi- buffered formaldehyde or paraformaldehyde- tionally, as indicated by Arratia (’87), ‘‘de- glutaraldehyde. Clearing and staining fol- tailed ontogenetic studies of different struc- lowed Hanken and Wassersug (’81) with tryp- tures in different groups are needed as base sin being replaced by a 1% KOH solution. for a future phylogenetic interpretation of These specimens were studied using a stereo- the relationships of the families of Siluroi- scopic microscope (WILD M5). Eight speci- dei.’’ mens were used for serial sectioning after TABLE 1. Specimens used for present study nr SL1 (mm) TL2 (mm) PAL 3 (mm) Age4 Method Staining5 Used for 1 4.1 4.4 2.3 1 clearing AB 1 ARS drawing 2 5.9 6.4 3.3 2 serial sections T 3D reconstructions 3 6.0 6.4 2.7 1 clearing AB 1 ARS drawing 4 6.6 7.0 3.2 2 clearing AB 1 ARS drawing 56 6.8 7.4 3.1 3 clearing AB 1 ARS observations 6 7.2 7.8 3.8 7 serial sections T 3D reconstructions 7 7.3 7.9 3.3 7 clearing ARS observations 8 7.7 8.7 3.7 9 clearing AB 1 ARS drawing 96 8.2 8.6 4.1 17 clearing AB 1 ARS observations 10 8.3 9.2 4.4 10 clearing ARS observations 116 8.4 9.1 4.2 13 serial sections T observations 126 9.3 10.7 4.9 21 clearing AB 1 ARS observations 136 10.0 11.3 5.0 21 clearing AB 1 ARS drawing 146 11.1 12.4 5.5 21 serial sections T observations 156 11.6 13.0 5.0 26 clearing AB 1 ARS drawing 166 12.0 13.5 6.2 26 clearing ARS drawing 176 12.7 15.0 6.1 26 clearing AB 1 ARS drawing 186 13.0 14.7 6.4 31 serial sections T observations 196 14.8 16.4 8.1 31 clearing ARS drawing 206 15.2 16.9 8.0 26 serial sections T observations 216 15.4 16.7 7.7 31 clearing ARS observations 226 15.5 17.8 8.3 31 clearing AB 1 ARS observations 236 18.7 20.9 9.2 31 serial sections T observations 246 19.0 21.1 11.1 31 clearing AB 1 ARS drawing 256 21.5 24.7 11.7 31 clearing AB 1 ARS drawing 26 46.8 50.2 23.9 119 serial sections T 3D reconstructions 27 125.5 144.9 67.1 100 clearing AB 1 ARS drawing 28 127.0 143.6 65.5 100 clearing AB 1 ARS drawing 29 140.1 158.4 72.4 100 clearing ARS drawing 30 174.5 187.7 90.9 ? clearing AB 1 ARS drawing IT 5 improved trichromous staining, T 5 T. 1Standard length. 2Total length. 3Preanal length. 4Number of days posthatching. 5AB 5 alcian blue; ARS 5 alizarine reds. 6Gynogenetic specimens. OSTEOCRANIUM ONTOGENY IN CLARIAS 185 embedding using Epon and Paraplast. The make a clear distinction between certain obtained 2 µm and 5 µm thick sections, bones and their margins. Serial microscopic respectively, were stained with toluidine and sections, however, revealed clearly the pres- an improved trichrome staining according to ence or absence of bones. The drawings were Mangakis et al. (’64). Sections were studied based on cleared material, so drawings of using a Leitz Diaplan light microscope. certain stages may not show the presence of Drawings of both cleared and sectioned ma- a certain bone, although that bone was al- terial were created using a camera lucida. ready observed in serial sections of a smaller Three-dimensional reconstructions of serial specimen. Despite this, the drawings do give sections were done using a commercial soft- ware package (PC3D, Jandel Scientific). a good representation of the morphology, as The examined specimens were obtained well as the chronology of ossification. from different egg batches. However, 17 of For anatomical references of the chondro- them belong to one single batch of gynoge- cranium, we refer to Adriaens and Verraes netical eggs, obtained by and according to (’97c), where the relation of the cranial bones Volckaert et al., (’94) (Table 1). with the cranial lateral-line system is dealt The present study uses body length as an with separately (Adriaens et al., ’97). The indicator of developmental stage. As several initiation of ossification of the cranial bones, factors such as temperature, prey size, prey grouped per region, is given in Table 2. The type, or water quality, may influence growth ontogeny of the Weberian apparatus is given rate, independent from age, growth itself is in the figures, but is not discussed here.
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