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Interspecific Variation of Body Shape and Sexual Dimorphism in Three Coexisting Species of the Genus Petrotilapia (Teleostei: Cichlidae) from Lake Malawi

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Interspecific Variation of Body Shape and Sexual Dimorphism in Three Coexisting Species of the Genus Petrotilapia (Teleostei: Cichlidae) from Lake Malawi Interspecific variation of body shape and sexual dimorphism in three coexisting species of the genus Petrotilapia (Teleostei: Cichlidae) from Lake Malawi Daud Kassam1*, Shinji Mizoiri2, and Kosaku Yamaoka1 1 Graduate School of Kuroshio Science, Kochi University, B 200 Monobe, Nankoku, Kochi 783-8502, Japan (e-mail: DK, [email protected]; KY, [email protected]) 22-22-7 Harada, Higashi Fukuoka, Fukuoka 812-0063, Japan (e-mail: [email protected]) Received: September 2, 2003 / Revised: February 17, 2004 / Accepted: March 5, 2004 Abstract Differences in color patterns have been the most used feature in describing cichlid species Ichthyological belonging to genus Petrotilapia from Lake Malawi. In this study, we quantified morphological variation Research in body shape within and among three coexisting Petrotilapia species using landmark-based geometric morphometric methods. Statistic analyses revealed significant body shape differences among species ©The Ichthyological Society of Japan 2004 but not between sexes. Post hoc multiple comparisons based on Mahalanobis distances revealed that P. Ichthyol Res (2004) 51: 195-201 nigra was significantly different from P. genalutea and Petrotilapia sp., whereas the latter two were not significantly different. The splines generated showed that the most pronounced variation was in the DOI 10.1007/s10228-004-0215-9 head region, in which P. nigra had a relatively longer and deeper head than the other two. The most clear-cut distinction was in gape length; P. genalutea had the longest gape, followed by Petrotilapia sp., whereas P. nigra had the shortest gape. Body depth was shallower in P. nigra than the others. When comparing sexes by their centroid size, ANOVA revealed that males were bigger than females. There­ fore, we conclude that color is not the only feature that can distinguish these congeners. We discuss the observed sexual dimorphism in terms of sexual selection and relate morphological variation among species to feeding behavior, which may help explain their coexistence in nature. Key words Sexual dimorphism • Coexistence • Epilithic algal feeder • Geometric morphometrics Thin-plate spline he adaptive radiation and explosive speciation dis trophically through food size partitioning, quantitative dif­ played by the cichlid fishes in the East African Great ferences in food composition, differences in food-collecting LakesT (Tanganyika, Malawi, and Victoria), continue to at­ strategies, and feeding microhabitat niche partitioning tract considerable interest. Lake Malawi, a younger lake (Yamaoka, 1982, 1997; Witte, 1984; Goldschmidt et al., 1990; than Lake Tanganyika, is estimated to harbour 800 cichlid Reinthal, 1990; Yuma, 1994; Kohda and Tanida, 1996; species, of which 99% are endemic (Snoeks, 2000). Further, Genner et al., 1999a,b). Such fine-scale segregation is be­ all these species are believed to have evolved from a lieved to partly explain the coexistence of many cichlid common ancestor within the last 700000 years (Meyer et al., species (Yamaoka, 1997; Genner et al., 1999a,b). In most 1990). This ancestor is said to have been a generalized cases, such trophic groups are identified by structural differ­ cichlid that diverged into two major clades, the rock- entiation of trophic morphology, even though such differen­ dwelling, locally known as Mbuna, and the sand-dwelling tiation is related more to the way the food is processed than (Moran et al., 1994; Seehausen et al., 1999). Rapid morpho­ to the type of food itself (Barel, 1983; Yamaoka, 1997). logical and behavioral evolution of the group has led to Witte (1984) stated that species that are virtually identical in adaptation to very divergent macrohabitats. Characteristics general aspects can, at a finer level, exhibit structural differ­ that have diverged between these ecomorphs include body ences which are related to differences in ecological de­ shape, trophic morphology, melanin patterning, reproduc­ mands. Hence, a morphological approach is perhaps one of tive behavior, and habitat preference (Fryer, 1959; Ribbink the ways of understanding the factors enhancing the coex­ et al., 1983). istence of cichlids. It is known that along Lake Malawi’s rocky shores these In this study, we used three coexisting Mbuna species cichlids are found at very high densities (ca. 20 adults/m2; belonging to the epilithic algal feeding genus Petrotilapia see Ribbink et al., 1983), which might generate intense com­ (endemic to Lake Malawi). The three species are petition for food as well as for other limited resources such Petrotilapia genalutea Marsh 1983, Petrotilapia nigra Marsh as space. However, thorough investigations have revealed 1983, and the undescribed Petrotilapia sp. referred to as that cichlids, including those from other lakes, segregate Petrotilapia “mumbo blue” (see Konings, 1990). The three 196 D. Kassam et al. species coexist along the shallower rocky shores where they feed on sediment-free biocover (Konings, 1990). It is thought that these species can only be distinguished through their coloration and that other aspects of their morphology remain relatively constant (Ribbink et al., 1983; Konings, 1990; Axelrod, 1993). We chose to test this assertion by investigating whether some morphological features of body shape exist that can be used to distinguish among the three species. Additionally, the fact that these three congeners coexist in the same habitat affords the opportunity to inves­ tigate possible ecomorphological links between morpho­ logical differentiation and partitioning of food resources. The color phenomenon has helped not only in distingushing species but also in sexual dimorphism. Despite the reported Fig. 1. Landmarks collected from the left side of the fish. 1, anterior tip diversity in trophic morphology (Fryer and Iles, 1972; of snout; 2, posterior extremity of the gape; 3, 4, anterior and posterior Yamaoka, 1982, 1997; Witte, 1984) and other body shape insertion of the dorsal fin; 5, 7, upper and lower insertion of caudal fin attributes (Ruber and Adams, 2001; Kassam et al., 2002, (angle point between body line and caudal fin); 6, posterior extremity 2003a,b) in other cichlid species, no such study has been of the lateral line; 8, 9, posterior and anterior insertion of the anal fin; done on Petrotilapia species. We therefore investigated the 10, insertion of the pelvic fin; 11, ventral insertion of the operculum on body shape variation among and within these three species the profile; 12, upper insertion of pectoral fin; 13, posterior extremity of to determine whether they may be distinguished by general the operculum body form alone. Hence the main objective in this study is to answer the nates of 13 homologous landmarks (Fig. 1) were digitized following questions. (1) Besides coloration, are there ana­ from the left side of each individual using TPSDIG version tomical features, in terms of body shape and size, that can be 1.17 (Rohlf, 1999a). The biological names and descriptions used to distinguish these species as well as sexes? (2) How of each landmark used can be found in the legend of Fig. 1. do the three species vary in their allometric trends? These landmarks were chosen for their capacity to cap­ ture overall body shape. Unfortunately, direct analysis of the landmark coordinates is not possible, as they contain Materials and Methods components of both shape and nonshape variation. To obtain shape variables, nonshape variation in the landmark Sample collection.—In April 2001, three Petrotilapia coordinates was removed by superimposing them using a species were collected from West Thumbi Island in the Generalized Procrustes Analysis (GPA) (Rohlf and Slice, Cape Maclear region of Lake Malawi (14°00' S 34°50' E). 1990). GPA removes nonshape variation by scaling all speci­ The following species were deposited at the marine center, mens to unit size, translating them to a common location, Usa, Kochi University; Petrotilapia genalutea (UKU and rotating them so that their corresponding landmarks 387002001-387002030, 75.9-116.4mm standard length (SL), line up as closely as possible. By using the thin-plate spline 16 males and 14 females), Petrotilapia sp. (UKU 387002031­ equation (Bookstein, 1989, 1991) and the standard formula 387002060, 85.3-139.9mm SL, 27 males and 3 females), and for uniform shape components (Bookstein, 1996), we ob­ P nigra (UKU 387002061-387002090, 68.9-113.4mm SL, 17 tained a weight matrix (containing uniform and nonuniform males and 13 females). Scuba divers, using hand nets and shape components) from the aligned specimens. Together, gill nets, captured adult fishes. Immediately after capture, the uniform and nonuniform components are treated as a fishes were placed in 10% formalin solution. Each specimen set of shape variables for statistical comparisons of shape also received an injection of formalin solution into the variation within and among groups (Caldecutt and Adams, body cavity, and all specimens were later transferred to 70% 1998; Adams and Rohlf, 2000; Ruber and Adams, 2001; ethanol. Kassam et al., 2003a,b). The foregoing procedures were Geometric morphometries and statistical analyses.— implemented in TPSRELW version 1.21 (Rohlf, 1999b). Cichlid body shape was quantified using landmark-based Variation in shape within and among species was evalu­ geometric morphometric (GM) methods (Rohlf and ated using several statistical procedures. First, to determine Marcus, 1993). GM methods are preferable to linear dis­ if shape varied significantly among species and between tance methods because the geometric relationships among sexes, and also to explore the effect of body size on body the variables are preserved throughout the analysis. Thus, in shape (i.e., allometry), a multivariate analysis of covariance additional to a statistical assessment of shape differences, (MANCOVA) was performed in which size was defined graphical representations of shape change can be presented. by as centroid size. Bookstein (1991) defined centroid size Images of each of the 90 specimens were taken using an as the square root of the sum of the squared distances of a OLYMPUS digital camera, with a resolution of 3.3 set of landmarks from their centroid. In this MANCOVA, megapixels.
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