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Ecomorphological Individual Variation in a Population of Haplochromis Nyererei from the Tanzanian Part of Lake Victoria

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Ecomorphological Individual Variation in a Population of Haplochromis Nyererei from the Tanzanian Part of Lake Victoria Journal o f Fish Biology (1998) 53, 66-83 Article No.jb980674 Ecomorphological individual variation in a population of Haplochromis nyererei from the Tanzanian part of Lake Victoria Y. F erm on*^ and C. C ibertI *Laboratoire d ’Ichtyologie generale et appliquee Museum National d ’Histoire Naturelle, 43 rue Cuvier, F-75231 Paris cedex 05, France and ILaboratoire de biologie du developpement, Institut Monod, CNRS, Universite Paris VII, Tour 43, 2 place Jussieu, F-75005 Paris, France (Received 2 July 1997, Accepted 19 February 1998) Intraspecific morphological variation among a population of Haplochromis nyererei (Teleostei, Cichlidae) from Lake Victoria was investigated. Three main groups of variables were used: general shape, outline of the head, and trophic group (intestinal length, stomach contents, teeth and jaw shape, lower jaw length and width). Fishes were arranged into four groups: G1, large males with a prominent bump on the head, a thickset body and anatomical structures related to a strictly insectivorous diet; G2, large males lacking a bump on the head but more or less thickset and showing anatomical structures related to omnivorous feeding habits, though favouring insects; G3, males and a few females with a slight bump on the head, a slender body shape and showing anatomical structures related primarily to a herbivorous tendency; and G4, females and a few small males without a bump on the head, a slender body and showing anatomical structures related to an omnivore with herbivorous tendencies. Several hypotheses related to behaviour are presented partly to explain the intraspecific variation observed. Differences between individuals could arise as a result about the establishment of dominance and territory in males. © 1998 The Fisheries Society of the British Isles Key words: Haplochromis nyererei; Cichlidae; Lake Victoria; rocky shores; ecomorphology; phenotypic plasticity. INTRODUCTION Ecomorphology studies the relationships of functional morphology and ecology. It is based on the premise that the morphological features of an animal are related to its ecology (Block et al., 1991). Morphological features are variables that describe and allow one to compare shapes of organisms in ecological or evolutionary studies (Motta & Kotrschal, 1992). Taxonomic investigations deal mainly with the identification and classification of organisms based on differ­ ences in morphological features. This is difficult when working with groups of closely related species. Several groups of fishes exhibit a remarkable range of morphological adaptive radiation. One of the most famous examples is that of the cichlid fishes, especially those of the Great Lakes of Africa: Victoria, Tanganyika and Malawi (Fryer & Iles, 1972; Greenwood, 1974, 1981). Fishes from these lakes show extremely diverse specialization in the anatomy of their feeding structures ^Author to whom correspondence should be addressed. Tel.: 33 1 40 79 37 36; fax: 33 1 40 79 37 71; email: [email protected] 66 0022-1112/98/070066+18 $30.00/0 © 1998 The Fisheries Society of the British Isles INDIVIDUAL VARIATION IN HAPLOCHROMIS NYEREREI 67 (Greenwood, 1974, 1981; Witte & van Oijen, 1990). This diversity reflects the cichlids’ ability to specialize with respect to certain kinds of food. Taxonomic features used to describe these species are related usually to these anatomical feeding structures, such as the lower jaw teeth, lower pharyngeal teeth, size of the lower jaw, gut length, and body form (Witte & van Oijen, 1990). The usual characteristics assessed are of a morphometric (the distance between two anatomical landmarks), meristic and qualitative nature (tooth shape and settings). The probably monophyletic flock of Lake Victoria (Sage et al., 1984; Meyer et al., 1990; Lippitsch, 1993) comprises nearly 200 described and many undescribed species of haplochromine cichlid fishes (Greenwood, 1974, 1981; van Oijen, 1996). Some of these display high phenotypic plasticity (Barel et al., 1976; Witte et al., 1990; Huysseune et al., 1994). Analysis of these species requires a multiplicity of variables in order to group the individuals into higher taxa (Barel et al., 1977; Greenwood, 1981; Snoeks et al., 1987a,b; van Oijen, 1996). Each species may have a high range of morphological variation that overlaps characteristics of other species. Differences are frequently greater among individuals of the same species than among closely related species of the same community (Greenwood, 1981; Hoogerhoud et al., 1983). According to Mayr (1974), this stage of morphological differentiation has to correlate with other biological features such as behaviour, ecology and physiology. However, little is known about the effect of environmental factors on phenotypic plasticity at later stages of ontogeny (Witte et al., 1990). In conducting analysis to understand the functioning of communities of the haplochromines of Lake Victoria, four questions which must be addressed. (1) Is it possible to separate different species according to their morphological features (morphometric, meristic, and qualitative)? (2) Which characteristics are best suited? (3) If not, which other characters could provide a more powerful discriminant between individuals? (4) What are the intraspecific morphological variations? This study was the first attempt to address these questions by combining several variables relative to the morphology of a single population of Haplochromis nyererei Witte-Maas & Witte, a lithophilous species. The first step consisted of the definition of significant morphological differences between individuals of different sex and age. Three groups of measurements were used: (1) the trophic features (intestinal length, stomach contents, teeth and jaw shape, lower jaw length and width); (2) the morphometrics of body structures; and (3) the outline of the head. The parameters which allow the best intraspecific differences between the individuals were determined. Using a multivariate statistical method an intraspecific behavioural significance is proposed between morphology and ecology of the animals of the present sample. MATERIALS AND METHODS RESEARCH AREA AND SAMPLING TECHNIQUES Haplochromis nyererei were collected in 1991 in the Tanzanian part of Lake Victoria at Nyamatala Island in the Mwanza Gulf, during an overall sampling programme in collaboration with the HEST Team (Haplochromis Ecology Survey Team) of the 68 Y. FERMON AND C. CIBERT University of Leiden (The Netherlands). Nyamatala Island is a rocky island covered by vegetation situated near to the eastern shore of the Mwanza Gulf, 15 km south of the town of Mwanza, at 2°44' S, 32°58' E. Fishes were captured using a battery of gillnets (mesh-size 2 5—5 cm) and by angling with earthworm baits. All 41 males and 18 females were captured at a maximum depth of 2 m. These were placed immediately on ice to prevent decomposition of the stomach contents. All viscera were removed subsequently and preserved separately for stomach contents analysis. The fishes were preserved in 80% alcohol after fixing in 8% formaldehyde and kept in the collection at the Museum National d’Histoire Naturelle of Paris, France. Haplochromis nyererei show a high range of variation in coloration and morphology in relation to their trophic habits and location in the Mwanza Gulf (Fermon, 1996; Seehausen, 1996, 1997). To avoid mistaken identification of the form or species, only red fish were used (normal form) as described by Witte-Maas & Witte (1985), caught around a single island. Fishes were identified in the field on the basis of colour patterns. Further precise taxonomic investigations were made according to the description of H. nyererei by Witte-Maas & Witte (1985). Morphometric measurements, meristic characteristics and counts were taken according to previous studies on cichlid fishes (Barel et al, 1977; Greenwood, 1981; Snoeks et al., 1987a; Snoeks, 1994). TROPHIC GROUP DETERMINATION Stomach contents were examined under a binocular microscope and quantified according to the procedure of Hynes (1950), Lauzanne (1977) and Hyslop (1983). Intestinal length (LI) that shows a relationship to diet (Greenwood, 1981) was measured. Lower jaw length (LLj), lower jaw width (WLj), upper jaw length (Luj) and premaxillary pedicel length (LPP) were also used for trophic group determination (Witte & van Oijen, 1990). The tooth band and the teeth were described carefully because of their taxonomic importance and the direct relationships between diet and jaw morphology (Barel et al., 1977; Greenwood, 1981). Jaw characteristics were analysed first. The shape of the dental arcade in lower and upper jaws provides 10 characters. The teeth of the outer and the inner rows in both jaws contribute a further 86 characters. Several of these were considered as specific (Witte-Maas & Witte, 1985). Then, the relationship between stomach contents and intestinal length was studied. MORPHOMETRICS An apparatus was constructed to collect data (Fermon, 1996). Landmarks were used to describe body shape (Strauss & Bookstein, 1982) (Fig. 1). The main principle of this apparatus is to focus each landmark under a binocular microscope. The positioning gear was accurate to 1 |im and the reproducibility of a landmark was 98%. Each fish was fixed on the support with all fins spread out and the mouth closed. The co-ordinates of each point were entered directly into a PC computer. Twenty-five landmarks were used to calculate and compute the distances between them. Thirty-seven morphometric parameters were measured (excluding
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