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Development of the Chondrocranium in the Suckermouth Armored Catfish Ancistrus Cf

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Development of the Chondrocranium in the Suckermouth Armored Catfish Ancistrus Cf JOURNAL OF MORPHOLOGY 266:331–355 (2005) Development of the Chondrocranium in the Suckermouth Armored Catfish Ancistrus cf. triradiatus (Loricariidae, Siluriformes) Tom Geerinckx,* Marleen Brunain, and Dominique Adriaens Evolutionary Morphology of Vertebrates, Ghent University – UGent, 9000 Ghent, Belgium ABSTRACT The chondrocranium of the suckermouth family is the largest within the Siluriformes and is armored catfish Ancistrus cf. triradiatus was studied. Its renowned for its remarkable niche occupation, i.e., development is described based on specimens ranging the scraping and sucking of algae and other food from small prehatching stages with no cartilage visible, to types off various substrates. Within the superfamily larger posthatching stages where the chondrocranium is reducing. Cleared and stained specimens, as well as serial Loricarioidea, the loricariids developed a highly spe- sections, revealed a cartilaginous skeleton with many fea- cialized feeding apparatus, with a ventral suctorial tures common for Siluriformes, yet several aspects of A. cf. mouth, tilted lower jaws, and new muscle configu- triradiatus are not seen as such in other catfishes, or to a rations that greatly increase jaw mobility as the lesser extent. The skull is platybasic, but the acrochordal most eye-catching adaptations (Alexander, 1965; cartilage is very small and variably present, leaving the Schaefer and Lauder, 1986). A number of studies notochord protruding into the hypophyseal fenestra in the have focused on the group, clarifying many aspects earlier stages. The ethmoid region is slender, with a rudi- of the adult osteology and myology of the Loricari- mentary solum nasi. A lateral commissure and myodomes idae (a.o. Howes, 1983; Schaefer, 1987, 1988; are present. The larger posterior myodome is roofed by a prootic bridge. The maxillary barbel is supported by a Schaefer and Lauder, 1986). conspicuous cartilaginous rod from early prehatching Many questions concerning loricariid morphology stages. The ceratohyal has four prominent lateral pro- are still unresolved. Virtually nothing is known cesses. Infrapharyngobranchials I–II do not develop. Dur- about their ontogeny. One aspect was studied by ing ontogeny, the skull lengthens, with an elongated eth- Carter and Beadle (1931), who confirmed the devel- moid, pointing ventrally, and a long and bar-shaped opment and function of the stomach as a respiratory hyosymplectic-pterygoquadrate plate. Meckel’s cartilages organ in Liposarcus anisitsi. A critical question is point medially instead of rostrally. J. Morphol. 266: whether a family with such aberrant adult head 331–355, 2005. © 2005 Wiley-Liss, Inc. morphology shows the general siluriform tendencies KEY WORDS: ontogeny; skeleton; cartilage; Ancistrus; during early development. Given the atypically silu- Loricariidae; catfishes riform adult morphology of Loricariidae, coupled with a peculiar, not completely understood feeding and respiratory behavior, one could question how this affects early life stages. In addition, hatchlings The ontogeny of fishes and other vertebrates mer- appear to be able to adhere themselves to the sub- its attention for various reasons. First, a description strate immediately, using their sucker mouth, as of ontogeny and ontogenetic transformations is es- noted by Riehl and Patzner (1991) in the loricariid sential for understanding the pattern behind body Sturisoma aureum. A first step in answering ques- plan formations. Second, this knowledge provides tions concerning ontogeny and function in Loricari- information that can be used in reconstructing phy- idae, and hence the ontogeny of function, is a proper logenies. Third, attention must be given to the fact that an organism must be functional at each mo- ment, including young, growing, ever-changing, and thus “temporary” stages (Galis, 1993; Galis et al., Contract grant sponsor: Institute for the Promotion of Innovation 1994). Organisms can hardly be understood by con- through Science and Technology in Flanders (IWT-Vlaanderen) (PhD grant to T.G.); Contract grant sponsor: FWO; Contract grant number: sidering only their adult forms, and study of their G.0355.04. early ontogeny may be more revealing and is there- fore very important (Balon, 1986). *Correspondence to: Tom Geerinckx, Evolutionary Morphology of An interesting case, of which very little is known Vertebrates, Ghent University – UGent, K.L. Ledeganckstraat 35, at the moment, is the ontogeny and growth in the 9000 Ghent, Belgium. E-mail: [email protected] catfish family Loricariidae, or suckermouth armored Published online 18 October 2005 in catfishes. With more than 670 species (Ferraris et Wiley InterScience (www.interscience.wiley.com) al., 2003), this extremely diverse South American DOI: 10.1002/jmor.10381 © 2005 WILEY-LISS, INC. 332 T. GEERINCKX ET AL. TABLE 1. Specimens of Ancistrus cf. triradiatus used in the present study No. SL (mm) SkL (mm) Age (PF) Method Staining Used for 1 4.8 — 2 Serial sections T Observation 2 5.2 — 3 Serial sections T 3D reconstruction 3 5.6 1.24 4 Clearing AB ϩ AR Drawing 4 6.0 1.39 4 Clearing AB ϩ AR Drawing 5 6.1 — 4 Serial sections T Observation 6 6.3 1.47 5 Clearing AB ϩ AR Observation 7 6.8 1.60 5* Clearing AB ϩ AR Drawing 8 7.0 — 6 Serial sections T Observation 9 7.4 1.82 6 Clearing AB ϩ AR Drawing 10 7.7 2.00 6 Clearing AB ϩ AR Observation 11 8.0 2.16 7 Clearing AB ϩ AR Drawing 12 8.0 — 7 Serial sections T Observation 13 8.5 2.38 7 Clearing AB ϩ AR Observation 14 8.7 2.45 7 Clearing AB ϩ AR Observation 15 8.9 2.51 8 Clearing AB ϩ AR Drawing 16 9.9 2.82 10 Clearing AB ϩ AR Drawing 17 10.2 — 14 Serial sections T Observation 18 11.5 3.38 30 Clearing AB ϩ AR Observation 19 12.4 — 43 Serial sections T Observation 20 12.7 3.67 48 Clearing AB ϩ AR Observation AB: alcian blue, AR: alizarin red S, PF: post-fertilization, SL: standard length, SkL; chondrocranial skull length (from tip of ethmoid plate to end of basis of occipital pilae, thus excluding tectum posterius), T: toluidine blue. *Immediately after hatching. knowledge of the changing morphology during on- MATERIALS AND METHODS togeny. This article deals with the development and Ancistrus cf. triradiatus Eigenmann, 1918 (a bristlenose cat- growth of the chondrocranium in a representative fish) was chosen for this study because of its fairly typical lori- loricariid species, the “bristlemouth” suckermouth cariid habitus and medium size. Until recently, Ancistrinae was armored catfish Ancistrus cf. triradiatus. recognized as one of six subfamilies in the Loricariidae (de Pinna, The chondrocranium of several of the ϳ34 silu- 1998). Armbruster (2004) lowered the Ancistrinae to the tribe riform families has already been described. Ac- Ancistrini in the subfamily Hypostominae. The systematics within the Ancistrini remain largely unresolved (de Pinna, 1998; counts of one or more stages in the development of Armbruster, 2004). Complete determination keys of Ancistrus the chondrocranium are published for Ariidae itself are nonexistent, and the genus is in need of revision. (Ariopsis felis; Bamford, 1948; Arius jella; Srini- Specimens representing the major period of the early ontogeny vasachar, 1958a), Bagridae (Mystus vittatus, Rita were used to study the morphology of the chondrocranium, from early prehatching stages (no cartilage visible) to later stages in sp.; Srinivasachar 1957a), Callichthyidae (Calli- which the osteocranium becomes predominant. Various egg chthys callichthys; Hoedeman, 1960; Hoploster- clutches were obtained from adults kept in a 24–26°C aquarium; num littorale; Ballantyne, 1930), Clariidae (Clar- all specimens were fathered by the same male. At different time ias gariepinus; Vandewalle et al., 1985; Surlemont intervals eggs and embryos were sedated in MS-222 and fixed in et al., 1989; Surlemont and Vandewalle, 1991; a paraformaldehyde-glutaraldehyde solution. For prehatching stages, egg scales were removed prior to fixation. Most specimens Adriaens and Verraes, 1994, 1997a; Heterobran- were used for in toto clearing and staining following the alcian chus longifilis; Vandewalle et al., 1997), Clarotei- blue / alizarin red method of Taylor and Van Dyke (1985) (Table dae (Chrysichthys auratus, Vandewalle et al., 1). Examination of the specimens was done using an Olympus 1999), Heteropneustidae (Heteropneustes fossilis; SZX9 stereoscopic microscope equipped with a camera lucida for drawing. Seven specimens were selected for serial sectioning. Srinivasachar, 1958b, 1959), Ictaluridae (Ameiu- Toluidine blue-stained 2-␮m sections (Technovit 7100 embed- rus nebulosus; Kindred, 1919), Pangasiidae (Pan- ding, cut with a Reichert-Jung Polycut microtome) were studied gasius pangasius; Srinivasachar, 1957b), Plotosi- using a Reichert-Jung Polyvar light microscope. A 3D reconstruc- dae (Plotosus canius; Srinivasachar 1958a), tion was made from serial sections of the 5.2 mm stage using the Schilbeidae (Ailia coila, Silonia silondia; Sriniva- software package Amira 3.1.1 (TGS Europe, France). sachar 1957b), and the suspensorium of Trichomy- cteridae (Arratia, 1990). Recent articles have shed RESULTS light on generalities and trends, as well as the diversity in catfish chondrocrania (Arratia, 1992; The chondrocranium of Ancistrus cf. triradiatus is Adriaens and Verraes, 1997a; Vandewalle et al., composed of cell-rich hyaline cartilage (Benjamin, 1999; Adriaens and Vandewalle, 2003). The cur- 1990). Both appositional growth (proliferation of rent study of the chondrocranium of a species of chondroblasts at the outer edge
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