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Teleostei, Perciformes) Animal Biology, Vol. 56, No. 3, pp. 351-372 (2006) Koninklijke Brill NV, Leiden, 2006. Also available online - www.brill.nl A preliminary study of development of the buccal apparatus in Pomacentridae (Teleostei, Perciformes) B. FREDERICH ∗, E. PARMENTIER, P. VANDEWALLE Laboratoire de Morphologie fonctionnelle et évolutive, Institut de Chimie (B6), Université de Liège, B-4000 Liège, Belgium Abstract—This study compares, in five species of Pomacentridae (Chromis viridis, Dascyllus flavicaudus, Chrysiptera glauca, Pomacentrus pavo, Plectroglyphidodon lacrymatus), the changes in cephalic skeletal structures between settling larvae and adults living on the reef. Variations were studied in the suspensorium, the opercle, the mandible, the premaxillary bone and the teeth. Comparisons of the feeding apparatus enabled two different types of feeding to be distinguished in adults: suction feeding and grazer sucking. Adult C. viridis and D. flavicaudus haveahigh suspensorium, a well-rounded mouth during jaw opening and caniniform teeth. These two species can be considered to be suction feeders. On the other hand, adult C. glauca, P. pavo and P. lacrymatus have less developed suspensoria, opercles and ascending process of the premaxillar, and present incisiform teeth. These three species appear to be grazer suckers. However, the larvae of all five species present an unimodal way of feeding, defined as ram-suction. Differences between larvae and adults appear clearly to be related to their ecology. The increasing variation presented in feeding apparatus during the settlement phase could be linked to diversification leading to occupancy of different ecological niches. Keywords: Ecomorphology; larvae; metamorphosis; Pomacentridae. INTRODUCTION The Pomacentridae family, or damselfishes, includes more than 300 species living mainly in a coral reef environment (Allen, 1991; Nelson, 1994). Pomacentrids have been studied with reference to their systematics (Randall and Allen, 1977), to their ecology (Sale, 1976; Lobel, 1980; Montgomery, 1980; Williams, 1980; Meekan et al., 1995; Letourneur et al., 1997) and to their behaviour (Ormond et al., 1996; Fishelson, 1998). The first anatomical descriptions of their morphology were made by Ciardelli (1967) and Emery (1973, 1980). Potthoff et al. (1987) also conducted a ∗Corresponding author; e-mail: [email protected] 352 B. Frederich, E. Parmentier, P. Vandewalle study of the osteological development of Microspathodon chrysurus (Cuvier). More recently, some authors have been interested in the functional morphology (Galis and Snelderwaard, 1997; Gluckmann and Vandewalle, 1998; Gluckmann et al., 1999) and in the phylogeny (Tang, 2001; Jang-Liaw et al., 2002; Quenouille et al., 2004) of these fishes. Most coral reef fish possess a complex life cycle involving a larval pelagic dis- persal period and a benthic life period that starts after settlement (McCormick and Makey, 1997; Leis and McCormick, 2002). This shift in habitat is a crucial phase leading to behavioural changes that can coincide with morphological modifications (McCormick et al., 2002; Parmentier et al., 2004). The majority of damselfishes have a planktonic larval phase (Allen, 1991). This life period lasts 2 to 5 weeks, depending on the species (Wellington and Victor, 1989). The ‘metamorphosis’, gen- erally coinciding with settlement (Leis and McCormick, 2002), mainly consists of acquisition of a bright colour and some morphological changes, such as modifi- cation of body shape (McCormick et al., 2002). Larvae are usually planktivorous, whereas juveniles and adults may have different diets (Drost et al., 1988) thus set- tlement phase can also correspond to changes in diet (Ciardelli, 1967; Letourneur et al., 1997). Moreover, in Microspathodon chrysurus, juveniles are mainly car- nivorous, whereas adults are algal browsers (Ciardelli, 1967). This change in diet and lifestyle during development should result in morphological modifications to the food capture system (Liem, 1991, 1993; Wagemans and Vandewalle, 2001). To date, no study has described the transformation of larval cephalic skeletal structures into adult structures in Pomacentridae. The aim of this study is to compare the buccal apparatus (premaxilla, suspensoria and opercules) of settling larvae and adults in five different pomacentrid species (fig. 1). These comparisons, realised in the framework of phylogenetic studies and ecological data, should provide insight into larval feature modification, and could bring an understanding of the adaptive radiation of this family on coral reefs. Species were selected on the basis of two criteria: biology of the adults specially characterized by their habitat and diet (table 1), and Allen’s classification (1991). Chromis viridis (Cuvier) and Dascyllus flavicaudus (Randall & Allen) are Chromi- nae. Chrysiptera glauca (Cuvier), Pomacentrus pavo (Bloch) and Plectroglyphi- dodon lacrymatus (Quoy & Guimard) are Pomacentrinae. According to Quenouille et al. (2004), Pomacentrinae can be divided into two clades: C. glauca and P. pavo belonging to one and P. lacrymatus to another. MATERIALS AND METHODS Specimens of each species were collected in Moorea (Society Islands, French Polynesia) in October 1997, July and August 1998, and November 1999. Adults were collected after the release of rotenone powder into the lagoon, or after exposure to a solution of quinaldine. During the same period, larvae were caught at night when they arrived on the reef crest. The net used (1.5 m wide × 0.75 m height × Buccal apparatus in Pomacentridae 353 Figure 1. a, Chromis viridis; b, Dascyllus flavicaudus; c, Chrysiptera glauca; d, Plectroglyphidodon lacrymatus; e, Pomacentrus pavo (pictures from Allen, 1991). 5 m length, 1 mm mesh) is similar to one used by Dufour et al. (1996). Samples were preserved in 10% formalin then transferred to 70% alcohol. Anatomical descriptions are based on the observation of dissected specimens. Some of these specimens were stained with alizarin red S, following Taylor and Van Dyke’s (1985) method. The following specimens were used: Chromis viridis: nine larvae (1 cm standard length, SL) and four adults (5-6 cm SL); Chrysiptera glauca: four larvae (1.5 cm SL) and four adults (5-7 cm SL); Dascyllus flavicaudus: two larvae (1.5 and 1.7 cm SL) and five adults (5-8 cm SL); P. pavo: seven larvae (1.5 cm SL) and five adults (5-6 cm SL); Plectroglyphidodon lacrymatus:twolarvae (1.5 cm SL) and five adults (4-5 cm SL). The individuals observed were drawn with a Wild M5 binocular microscope coupled to a camera lucida. To facilitate comparison, we referred the neurocranium 354 B. Frederich, E. Parmentier, P. Vandewalle Table 1. Biology of the five studied adult species. Diet Habitat Maximum References size (cm, SL) Chromis viridis Zooplankton feeder Inshore and lagoon reefs; 7 Allen, 1991 closely associated with branching corals, especially Acropora Dascyllus Omnivorous feeding Coral and rocky reefs 9 Randall and flavicaudus largely on Allen, 1977 zooplankton Chrysiptera glauca Omnivorous feeding Shallow reefs exposed 8 Kuo and Shao, largely on algae to wave action 1991 Pomacentrus pavo Omnivorous Sandy areas of lagoon 8.5 Allen, 1991 reefs, isolated patch reefs, coral heads or rubble Plectroglyphidodon Herbivorous Lagoon and seaward reefs, 8 Kuo and Shao, lacrymatus in areas with mixed 1991 coral and rubble or dead coral rocks of larvae and adults to the same reference length. This was the flat projection of the distance between the former extremity of the ethmoïd area to the posterior extremity of the basioccipital, when the orbital portion of the parasphenoid was placed horizontally. The other studied structures were adjusted with respect to the neurocrania. The teeth of the larvae and adults were dehydrated and underwent metallisation by Au-Pd pulverisation (Balzers SCD-30). Photographs were taken with a scanning electron microscope (Jeol, JSM840A) using an acceleration voltage of 19 kV. Lower jaw-lever mechanics were investigated in larvae and adult fish of the five species. This method allows the comparison of efficiency of the jaw closing and opening systems (Wainwright and Richard, 1995). It is based on three measurements and two ratios. Distance from the mid-point of the articular-quadrate joint to the mid-point of the interopercular bone-angular joint corresponds to the jaw opening in-lever (line c; fig. 2b). The in-lever for jaw closing is the distance between the mid-point of the articular-quadrate joint to the point of insertion of the adductor mandibulae muscle on the articulo-angular. In Pomacentridae, the bundle A3β of the adductor mandibulae is the wider muscle inserting on the articulo-angular (Gluckmann et al., 1999). Its insertion on the medial face of the lower jaw, on the coronomeckelien, was chosen in this analysis (line b, fig. 2b). The jaw closing out- lever is the distance between the mid-point of the articular-quadrate joint and the Buccal apparatus in Pomacentridae 355 Figure 2. Pomacentrus pavo adult. a, lateral view of the mandible. b, lateral view of the mandible illustrating the points of measurement for jaw lever arms. c, lateral view of the premaxillary bone. ANG, articulo-angular; A.PR, ascending process of the premaxilla; COR.PR, coronoïd process; COR, coronomeckelien; DENT, dentary; DENT.PR, dentigerous process; PMAX, premaxillary bone; RAR, retroarticular. anterior tip of the dentary (line a; fig. 2b). Dimensionless ratios were calculated for the jaw opening and closing systems: Jaw Opening Lever Ratio (JO) = jaw opening in-lever/jaw closing
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