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Body Shape Variation in Relation to Resource Partitioning

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Body Shape Variation in Relation to Resource Partitioning AnimalBiology ,Vol.53, No. 1, pp. 59-70 (2003) Ó KoninklijkeBrill NV ,Leiden,2003. Alsoavailable online - www.brill.nl Body shape variation inrelation to resourcepartitioning within cichlidtrophic guilds coexisting along the rocky shore of Lake Malawi 1; 2 3 DAUDD. KASSAM ¤,DEANC. ADAMS ,AGGREYJ.D. AMBALI , KOSAKUY AMAOKA 1 1 Departmentof Aquaculture,Kochi University, B 200Monobe, Nankoku-shi, Kochi, 783-8502, Japan 2 Programin Ecology and Evolution, Department of Zoology and Genetics, Iowa State University, Ames,Iowa 50010, USA 3 Departmentof Biology,University of Malawi, Chancellor College, P .O.Box 280, Zomba, Malawi Abstract—Toappreciatebetter how cichlids segregate along the trophic, spatial and temporal dimen- sions,it is necessary to understand the cichlids’ body design, and its role in resourcepartitioning. We investigatedbody shape variation, quanti ed usinglandmark-based geometric morphometrics, among cichlidspecies belonging to algaland zooplankton feeders coexisting along the rocky shores of Lake Malawi,in order to elucidate the adaptive signi cance of body shape. Signi cant differences were foundwithin zooplankton feeders in which Copadichromisborleyi hada shortergape, smaller eyes andshorter caudal peduncle relative to Ctenopharynxpictus and,within algal feeders, Labeotropheus fuelleborni hada shorterand inferior subterminal gape, and shorter head relative to Petrotilapiagena- lutea.Variationamong species is discussedwith reference to trophicand feeding microhabitat differ- entiationwhich enables us to appreciate the role of bodyshape in enhancing ecological separation, andthus leads to coexistenceamong cichlid species. Keywords:Cichlidae;geometric morphometrics; Lake Malawi; resource partitioning; trophic guild. INTRODUCTION Twoclassic hypotheseshave been posited to explainwhy there are manycichlid species in the AfricanGreat Lakes,viz.; LakesVictoria, Malawi andT anganyika (butsee Korneld andSmith, 2000).The rst states that the cichlid morphological design,particularly ofthe feedingapparatus, is akeyinnovation for rapid speciation ¤Correspondingauthor; e-mail: [email protected] 60 D.D. Kassamet al. (Liem,1973; Greenwood, 1991; Galis andMetz, 1998;but see Seehausen,2000). Thesecond promotes that sexual selection is the major forcedriving speciation (Turnerand Burrows, 1995; Seehausen et al., 1997).Though the twotheories seem to bein conict, ascientic approachembracing both ideas maybe the best way to understandwhy Cichlidae is the most speciose family in the Great Lakesof Africa (Galis andMetz, 1998).Sexual selection maybe a mechanism that produces reproductivelyisolated forms/species, butit falls short ofaccounting for the adaptive radiation that enables cichlids to exploit almost all available resources within the great lakes (Boutonet al., 1999).In addition to understandinghow cichlid radiation evolved,another important questionis: ecologically,howdo so manycichlid species coexist? Ribbinket al. (1983)reported that the haplochrominecichlids ofLake Malawi are foundat highdensities especially onthe rockyshore areas (e.g.,15 species at West ThumbiIsland with ca.20 adults/ m 2/ andHori et al. (1983)found manyadult shes (13species with ca.18/ m 2/ inhabitingthe rockyshores ofLake Tanganyika.Such high densities suggest intense competition forspace as well as forfood resources. Therefore, the wayin whichthese cichlids partition available resources is likely to beone of the main factors that enhancetheir coexistence. Cichlids, like other shes, are knownto partition resources in three major di- mensions namely; trophic,spatial andtemporal (Witte, 1984;Ross, 1986;Bouton et al., 1997).Trophically ,cichlids segregate throughfood size partitioning,quanti- tative differences in foodcomposition, differences in foodcollecting strategies and feedingmicrohabitat nichepartitioning (Y amaoka,1982, 1997; Hori, 1983, 1991; Witte, 1984;Goldschmidt, 1990; Reinthal, 1990;Y uma,1994; Kohda and T anida, 1996;Genner et al., 1999a,b). In most cases, suchtrophic groups are identied bystructural differentiation oftheir trophicmorphology ,eventhough such differ- entiation is related moreto the waythe foodis capturedand processed than to the typeof foodconsumed (Barel, 1983;Y amaoka,1997). However, instead ofstudying the trophicapparatus, which has receivedmuch attention fromprevious researchers (e.g.,Reinthal, 1989;Albertson and Kocher, 2001), we investigated overall cichlid bodyshape. Differentiation in overall bodyshape tends to beignored,despite the fact that diversity in bodyshape has beenreported in this groupby Fryerand Iles (1972),and has beenshown to beimportant in the evolutionof some lineages of Tanganyikancichlids (e.g.,Rü ber and Adams, 2001). Inthis study,we used four species that coexist alongthe rockyshores ofLake Malawi representingzooplankton feeders ( Ctenopharynxpictus and Copadichromis borleyi),andepilithic algal feeders ( Petrotilapia genalutea and Labeotropheus fuelleborni ).Zooplanktonand algal feeders werechosen since theyare the most dominanttrophic guilds amongLake Malawi’ s cichlid shes. Ctenopharynxpictus is benthophagous,but also feeds fromthe water columnwhen zooplankton is in abundance(T .Sato,pers. comm.), while its counterpart Copadichromisborleyi is reportedto feedfrom the openwater (Ribbinket al., 1983;Konings, 1990). The twoalgal feeders favourshallow rockyareas, althoughthere is some segregation betweenthem suchthat L.fuelleborni is commonlyfound on the sediment-free, Therole of bodyshape in resource partitioning 61 wave-beatensides ofthe rocks(Ribbink et al., 1983;Konings, 1990). It is in the light ofthis partitioning offood (zooplankton versus algae) andfeeding microhabitat, that promptedus to conductthis studyin orderto investigate if there are any morphologicaldifferences amongspecies that mayre ect adaptivesigni cance of bodyshape to suchresource partitioning. Hence our main purposeis to answer the followingquestion; is there bodyshape variation amongthese species that can berelated to resourcepartitioning (i.e. trophicand spatial dimensions) andthus enhanceecological separation that mayfacilitate their coexistence? MATERIALS AND METHODS SCUBAdivers, using hand nets andgill nets, capturedthe followingspecies from West ThumbiIsland in the CapeMaclear regionof LakeMalawi (14 ±000S 34±500E): P.genalutea (n 30,standard length, SL, 75.9-116.4 mm, in April 2001)and Copadichromisborleyi D , Ctenopharynxpictus , L.fuelleborni (n 30per species, SL,64.2-127.5, 65.6-101.3, 69.7-104.2, respectively ,in NovemberD 2001). Fishes wereplaced in 10%formalin solutionsoon after captureand each specimen was injected with formalin.They were then transferred to 70%ethanol and stored until examination. Geometric morphometricand statistical analyses. Landmark-basedgeometric morphometric(GM) techniques (Rohlf and Marcus, 1993) were used to quantify cichlid bodyshape. GM methods are preferableto quantifyingbody shape over linear distances becausethe geometric relationships amongthe variables are pre- servedthroughout the analysis. Thus,in additionto astatistical assessment ofshape differences,graphical representations ofshape change can also bepresented. An OLYMPUSdigital camera,with aresolution of3.3 megapixels, was usedto take images ofall specimens. The x, y coordinatesof 12 homologous landmarks ( g. 1) weredigitised fromthe left side ofeach individual using the software TPSDIG32 (Rohlf,version 1.19, 2001). These landmarks were chosen for their capacity to cap- ture overall bodyshape. Unfortunately, direct analysis ofthe landmarkcoordinates is notpossible, as theycontain components of bothshape and non-shape variation. Toobtainshape variables, non-shapevariation (dueto size, location andorienta- tion) in the landmarkcoordinates was removedthrough the Generalised Procrustes Analysis (GPA)(Rohlfand Slice, 1990).GP Aremovesnon-shape variation byscal- ingall specimens to unit size, translating them to acommonlocation, and rotating them so that their correspondinglandmarks line upas closely as possible. Fromthe alignedGP Acoordinates,an overall average(consensus) con guration is estimated andused in later analyses. Shapevariables are thenobtained from the alignedspec- imens usingthe thin-plate spline (Bookstein,1989, 1991) and the standardformula forthe uniformshape components (Bookstein, 1996). T ogether,the uniformand non-uniformcomponents are treated as aset ofshape variables forstatistical com- parisons ofshapevariation within andamong groups (e.g., Caldecutt andAdams, 62 D.D. Kassamet al. Figure 1. Positionsof landmarks used to de ne body shape collected from the left side of each sh; 1.anteriortip of snout;2 and3. anteriorand posterior insertion of thedorsal n;4 and5. upper and lowerinsertion of caudal n;6 and7. posteriorand anterior insertion of the anal n;8. insertionof the pelvic n;9.insertionof the operculum on thepro le; 10. upper insertion of pectoral n;11. posterior extremityof the operculum; 12. posterior extremity of the gape. 1998;Adams and Rohlf, 2000; Rü ber and Adams, 2001; Kassam et al., in press). Inaddition to the overall consensuscon guration, we calculated the consensuscon- gurationsfor each individual group. These were used to generaterepresentations ofshape of each group relative to the overall meanshape. The above-mentioned procedureswere implemented with the software TPSRELW(Rohlf, version 1.24, 2002a). Several statistical procedureswere used to investigate variation amongspecies. First, to determine if bodyshape varied signi cantly amongspecies, amultivariate analysis ofvariance (MANOV
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