Interspecific variation of body shape and sexual dimorphism in three coexisting species of the genus (Teleostei: Cichlidae) from

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 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 . 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 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. Pins were placed in each specimen before im­ species and sex were used as main factors with centroid age acquisition and data collection to facilitate accurate size as a covariate, and all interactions between them placement of landmarks on all specimens. The x, y coordi- were included (species X sex, species X centroid size, Body shape variation in Petrotilapia 197 sex X centroid size). Pairwise multiple comparisons were mens on the first two relative warps, which accounted for performed to determine which species (if any) significantly 48.8% of the total variation in shape. The three species, differed from one another. These comparisons were based especially their mean specimens, can be discerned quite on generalized Mahalanobis distance (D2) from a canonical clearly along the RW 2 axis, where P. nigra is found on variates analysis (CVA). The critical a for these tests was the positive side of RW 2, whereas the mean specimens for adjusted using the Bonferroni procedure, where the original the other two species are found toward the negative side of a = 0.05 is divided by the number of comparisons (= 3); this RW 2. yielded a critical a = 0.0167, for an experiment-wise error To visualize the shapes associated with such differentia­ rate of a = 0.05. tion, thin-plate spline deformation grids were generated Second, variation in shape among species was examined representing the mean specimen for each species (Fig. 2). through the relative warp analysis (RWA) where the scaling The most pronounced variation was in the head region, in parameter (a) was set to 0.0 (Rohlf, 1993). When all shape which P. nigra had a relatively longer and deeper head than variables are included and a = 0, a relative warp analysis is the other two. However, P. genalutea had the shallowest simply a principal components analysis of shape. Using head among the three species. The most clear-cut distinction RWA, we generated an ordination in which shape variation among the species concerned the gape; P. nigra had the was described in as few dimensions as possible. To show shortest gape length followed by Petrotilapia sp., whereas differences among species, we included the mean specimen P. genalutea had the longest. The deformation grids also for each species in this plot. Thin-plate spline deformation indicated that P nigra had a shallower body depth than grids were then generated for these species means to facili­ the others. tate description of group differences. To visualize and describe allometric trends, we generated Finally, a two-way analysis of variance (ANOVA) was thin-plate spline grids for the smallest and largest fish for performed on centroid size to determine whether size dif­ each species (Fig. 3, using the TPSREGR version 1.22; fered among species or between the sexes. All ANOVA Rohlf, 1999c). From this, the allometric trend in both P. procedures were computed with JMP statistical package genalutea and Petrotilapia sp. seem qualitatively similar, version 3.2 (Sall et al., 1999); the CVA was performed in such that the gape increases and body depth increases as the NTSYS-PC version 2.1 (Rohlf, 2000). fish grow. In contrast, the gape gets relatively shorter and the body becomes more slender as P. nigra grows. These differences correspond to the major differences between Results species, and thus it appears that differences in allometric trajectories have heightened species differences as fish in­ Interspecific variation and sexual dimorphism in shape. crease in size. Results from MANCOVA revealed significant differences Interspecific variation and sexual dimorphism in size. among species but not between sexes and also identified The two-way ANOVA performed on centroid size revealed significant allometry of shape relative to size (Table 1). Fur­ significant differences among species (F = 14.25, ther, a significant interaction between size and species P < 0.0001), and between the sexes (F = 18.24, P < 0.0001), implied that the nature of the shape allometry differed but no significant interaction between these factors between species. Using the generalized Mahalanobis dis­ (F = 1.85, P = 0.1652). Pairwise comparisons among spe­ tances, Petrotilapia nigra was found to be significantly differ­ cies showed that Petrotilapia sp. was significantly different ent from both P genalutea and Petrotilapia sp. (D2 = 5.4431, from the others (Tukey-Kramer HSD test, P < 0.05), 6.7996, respectively) but P. genalutea and Petrotilapia whereas Petrotilapia nigra and Petrotilapia genalutea were sp. were not significantly different from each other not significantly different from one another (P > 0.05). (D2 = 4.2186). Figure 2 depicts an ordination of all speci­ From their mean centroid sizes, Petrotilapia sp. was found to

Table 1. Summary of multivariate analysis of covariance (MANCOVA) performed on shape variables

Factor Wilks’ A Fs NumDF DenDF P

Species 0.3078 2.2929 42 120 0.0002 Sex 0.7787 0.8119 21 60 0.6948 CS 0.5148 2.6933 21 60 0.0014 Species X sex 0.4719 1.3022 42 120 0.1357 Species X CS 0.2886 2.4612 42 120 <0.0001 Sex X CS 0.8027 0.7023 21 60 0.8139

Wilks’ A, test statistic; Fs, f ratio; NumDF, degrees of freedom of the numerator; DenDF, degrees of freedom of the denominator; P, probability value; CS, centroid size 198 D. Kassam et al.

Fig. 2. Scatter plot of the first two relative warps. Arrows indicate mean specimens (filled symbols) for each species and deformation grids associated with such mean specimens. PN, Petrotilapia nigra; P. sp., Petrotilapia sp.; PG, Petrotilapia genalutea

be the largest, followed by P. genalutea and then P. nigra. exception of the head region. The diversity in the head Again from mean centroid sizes, males were larger than region, including gape length, is very important in adaptive females; this trend was consistent in all species. radiation because it enables the cichlids to utilize many feeding niches (Fryer and Iles, 1972). At this point, a better question to ask is: Do the interspe­ Discussion cific variations in body shape revealed in this study have any functional role to play to enhance ecological separation Contrary to the common belief that species in the genus and thus facilitate coexistence among these congeners? As Petrotilapia can only be distinguished by color (which is of already mentioned, the three species are all epilithic algal limited practical value, because it only helps for in situ iden­ feeders, which, according to Konings (1990), feed from a tification of species or sexes, but it is still difficult to assign sediment-free biocover with the aid of their long, slender, females to certain species), this study has documented some mobile teeth, which have spatulate tips (Fryer and Iles, subtle morphological differentiation among species. Much 1972). Of the three types of feeding (biting, suction, and more important is the pronounced variation among species ram-feeding), these species can be said to employ a biting that has been detected in the head region, especially the technique. Biting can include pulling/pull-scraping and gape length. This observation is consistent with the report of scraping/combing techniques. The former removes the fila­ Fryer and Iles (1972), who observed that most cichlids tend mentous algae from the rocks while the latter removes dia­ to have restricted diversity in their body form, with the toms and detritus from the rocks or from the filamentous Body shape variation in Petrotilapia 199

Fig. 3. Shape deformations associated with change in cen­ troid size: smallest specimen (left deformation grids); largest speci­ men (right deformation grids). PN, Petrotilapia nigra; P. sp., Petrotilapia sp.; PG, Petrotilapia genalutea

algae (Bouton et al., 1998). Konings (1990) reported that Hence, from the variation in gape length that is important P. genalutea feeds on loose algae while P. nigra prefers in determining the feeding strategy of the three species, miniscule diatoms that are found attached to algal strands. it can be seen that such finer morphological differentiation Although in reality we expect some overlap of their diets, tends to lead to ecological separation of the species, which from these statements we suggest that the larger gape in P. we suggest promotes their coexistence. Genner et al. genalutea is more efficient in pulling/pull-scraping of loose (1999b) observed that territorial males of some cichlid spe­ algae while the smaller gape in P. nigra is well adapted for cies could let in intruders, especially those with different scraping/combing of diatoms from the substrate. trophic morphologies. Such observations may partly sup­ As for Petrotilapia sp., because not much has been re­ port the idea that different trophic morphologies lead to ported on its feeding preference, it may seem somehow different trophic specialization, which in turn will reduce difficult to assign it to a certain biting technique, although interspecific competition in coexisting species. Therefore, we are tempted to predict from its intermediate gape length our study suggests that gape size is an important feature that that it may be a generalist that employs either pulling/ can illuminate the variation in foraging techniques of these pull-scraping or scraping/combing depending on the situa­ congeneric coexisting species. tion (e.g., prey type and potential competitor available). The sexual size dimorphism revealed here is consistent Such prediction, together with the food preference of this with other findings that male fish are generally bigger than Petrotilapia sp., suggests that further study, incorporating females (Iguchi et al., 1991; Oliveria and Almada, 1995; Park field observations, is necessary to understand how it inter­ et al., 2001). In Lake Tanganyika cichlids, the most extreme acts with its congeners in the same environment. sexual dimorphism was observed in the shell-brooding 200 D. Kassam et al.

Lamprologus callipterus where males are more than 12 Fryer G (1959) The trophic interrelationships and ecology of some of times heavier than females (Schutz and Taborsky, 2000). the littoral communities of Lake Nyasa with special reference to the Even though the degree of sexual dimorphism is expected fishes and a discussion of a group of rock frequenting Cichlidae. Proc to depend on a balance of natural and sexual selection (see Zool Soc Lond 132:153-281 Schutz and Taborsky, 2000), in our study, as well as the Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa: studies mentioned above, sexual selection seems to be the their biology and evolution. Oliver and Boyd, Edinburgh most applicable explanation, as such dimorphism promotes Genner MJ, Turner GF, Barker S, Hawkins SJ (1999a) Niche segrega­ success in male-male competition or female choice (see tion among Lake Malawi fishes? Evidence from stable isotope signa­ tures. Ecol Lett 2:185-190 Fryer and Iles, 1972; Barlow, 2000). This success means that Genner MJ, Turner GF, Hawkins SJ (1999b) Foraging of rocky habitat only the bigger males will have the chance to mate with as cichlid fishes in Lake Malawi: coexisting through niche partitioning? many females as possible, because such males will be able to Oecologia (Berl) 121:283-292 defend their territories. Goldschmidt PT, Witte F, de Visser J (1990) Ecological segregation in Axelrod (1993) noted that the genus Petrotilapia requires zooplanktivorus species (Pisces: Cichlidae) from a scientist competent in modern molecular techniques to Lake Victoria. Oikos 58:343-355 differentiate between these fishes. Although molecular Iguchi K, Ito F, Ikuta K, Yamaguchi M (1991) Sexual dimorphism in the studies certainly are important for distinguishing many taxa, anal fin of ayu Plecoglossus altivelis. Bull Jpn Soc Sci Fish 57:1501­ we believe that much can be gained by examining morphol­ 1505 ogy using a more rigorous approach. In contrast to prior Kassam DD, Sato T, Yamaoka K (2002) Landmark-based morphomet­ assertions, the results of our study demonstrate that mor­ ric analysis of the body shape of two sympatric species, Ctenopharynx phology can be used to distinguish among Petrotilapia taxa. pictus and Otopharynx sp. “heterodon nankhumba” (Teleostei: By using morphological techniques that account for varia­ Cichlidae), from Lake Malawi. Ichthyol Res 49:340-345 tion in body shape (geometric morphometrics), we have Kassam DD, Adams DC, Ambali AJD, Yamaoka K (2003a) Body shape shown subtle, but consistent, differences among species. variation in relation to resource partitioning within cichlid trophic Further, such differences are localized to the head (and guilds coexisting along the rocky shore of Lake Malawi. Ani Biol specifically gape), suggesting that a more detailed study of 53:59-70 the trophic morphology of this group would be of value. Kassam DD, Adams DC, Hori M, Yamaoka K (2003b) Morphometric analysis on ecomorphologically equivalent cichlid species from Lakes Malawi and Tanganyika. J Zool 260:153-157 Acknowledgments We are grateful to Mr. Naoki Makimoto for his Kohda M, Tanida K (1996) Overlapping territory of benthophagous assistance in sample collection. The Malawi government through its cichlid fish, Lobochilotes labiatus, in Lake Tanganyika. Environ Biol Fisheries Department is also acknowledged for permitting us to collect Fishes 45:13-20 samples from Lake Malawi. Dr. Dean Adams deserves our heartfelt Konings A (1990) Ad Konings book of cichlids and all the other fishes thanks for constructive ideas and critical reading of the manuscript. We of Lake Malawi. 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