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, quantiŽ 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 signiŽ cance of body shape. SigniŽ 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 KornŽeld andSmith, 2000).The Ž 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 conict, ascientiŽc 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 Žshes (13species withca. 18/ m 2/ inhabitingthe rockyshores ofLake Tanganyika.Such high densities suggest intense competitionfor space 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 otherŽ shes, are knownto partition resources inthree 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 identiŽed 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 tobe ignored,despite the fact that diversity inbody shape 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 Žshes. 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 rocky areas, 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 inthe light ofthis partitioningof food (zooplankton versus algae) andfeeding microhabitat, that promptedus to conductthis studyin orderto investigate if there are any morphologicaldifferences amongspecies that mayre ect adaptivesigniŽ cance of bodyshape to suchresource partitioning. Hence our main purposeis toanswer the followingquestion; is there bodyshape variation amongthese species that can berelated toresource partitioning (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, 75.9-116.4mm, 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 ,inNovember D 2001). Fishes wereplaced in 10%formalin solutionsoon after captureand each specimen was injected with formalin.They were then transferred to70% 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 methodsare preferableto quantifying body shape over linear distances becausethe geometric relationships amongthe variables are pre- servedthroughout the analysis. Thus,in addition to astatistical assessment ofshape differences,graphical representations ofshape change can also bepresented. An OLYMPUSdigital camera,with aresolutionof 3.3 megapixels, was usedto take images ofall specimens. The x, y coordinatesof 12 homologous landmarks (Ž 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 tounit size, translating them toa commonlocation, and rotating them so that their correspondinglandmarks line upas closely as possible. Fromthe alignedGP Acoordinates,an overall average(consensus) conŽ 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 withinand among groups (e.g., Caldecutt andAdams, 62 D.D. Kassamet al.

Figure 1. Positionsof landmarks used to deŽ ne body shape collected from the left side of eachŽ sh; 1.anteriortip of snout;2 and3. anteriorand posterior insertion of thedorsal Ž n;4 and5. upper and lowerinsertion of caudalŽ n;6 and7. posteriorand anterior insertion of the anal Ž n;8. insertionof the pelvicŽ n;9.insertionof the operculum on theproŽ le; 10. upper insertion of pectoral Ž 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., inpress). Inaddition to the overall consensusconŽ guration, we calculated the consensuscon- Žgurationsfor each individual group. These were used to generate representations 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, todetermine if bodyshape varied signiŽ cantly amongspecies, amultivariate analysis ofvariance (MANOV A)was performed(e.g., Rohlf et al., 1996;Adams andFunk, 1997; Caldecutt andAdams, 1998; Kassam et al., in press). Secondly, pairwise multiple comparisonswere performed to determine whichspecies (if any)signiŽ cantly differedfrom one another. These were based on generalised Mahalanobisdistance ( D2/ froma canonicalvariates analysis (CVA)with the critical ® (0.05)for these tests beingadjusted usingthe Bonferroniprocedure. TPSSPLINsoftware (Rohlf,version 1.16, 2002b) was usedto generatethin-plate spline deformationrepresentations ofgroup means.

Supplementalmeasurements. Because oftheir signiŽcance in the feedingecol- ogyof Žshes (Fryerand Iles, 1972;Rü ber and Adams, 2001), the followingtradi- tional morphometriccharacters werealso measured; interorbital width,measured as the distance onthe dorsal part ofthe headgiving the least widthbetween bony marginof the left andright orbit; gapewidth, the distance betweenthe endsof the mouthslit onthe left andright side. All measurements weretaken by usingdigital Therole of bodyshape in resource partitioning 63 calipers to the nearest 0.1mm. Analysis ofvariance (ANOV A)was performedto determine if these characters differedsigniŽ cantly amongspecies. Finally,atwo-blockpartial least squares analysis was performedto investigate if there was anyassociation betweenbody shape and the twotrophic characters measured.Two-block partial least squares analysis is amultivariate correlation techniquethat describes the covariancebetween two sets ofvariables (e.g.,Rohlf andCorti, 2000;Rü ber and Adams, 2001). This analysis was performedin TPSPLS software (Rohlf,version 1.09, 2002c). JMP software (Sall et al., version3.2, 1998), and NTSYS-PC software (Rohlf, version1.80, 2000) were used for the ANOVAandCV Aanalyses, respectively.

RESULTS Bodyshape variation. SigniŽcant differences in bodyshape among species were revealedthrough MANOV A(Wilks’ 3 0:0040283, F 27:536, P < 0:0001/. Plannedpairwise comparisonsamong species D usingGeneralised D Mahalanobisdis- tances indicated signiŽcant differences inbody shape among all species (table 1). Tovisualise shapedifferences, thin-plate spline deformationplots weregenerated forthe averagespecimen foreach species forboth zooplankton feeders (Žg. 2a, b) andalgal feeders (Žg. 2c,d). Forthe zooplanktonfeeders, Copadichromisborleyi hada shorter gape,a shorter butdeeper head, and a shorter caudalpeduncle relative to Ctenopharynxpictus . Ad- ditionally,the ventof Ctenopharynxpictus was moreanteriorly positionedrelative to that of Copadichromis borleyi (Žg. 2a,b). For the algal feeders, L.fuelleborni had ashorter andinferior subterminal gape,a shorter head,and a moreanteriorly placed pectoral Žnrelative to P.genalutea (Ž g. 2c, d).

Supplementalmeasurements. ANOVArevealedsigniŽ cant differences in the trophiccharacters amongthe species ( F 55:539, df 4, P < 0:0001/. The post- hocmultiple pairwise comparisonsindicated D that thereD was signiŽcant difference ininterorbital widthbetween zooplankton feeders (Tukey-Kramertest, P < 0:05, table 2),where Copadichromis borleyi hada larger interorbital width(mean § Table 1. Pairwisecomparisons based on GeneralisedMahalanobis distances among the four species belonging toalgal and zooplankton trophic guilds. All pairs are signiŽ cantly different (at ® 0:05, after D Bonferronicorrection) since the calculated critical D2 was 4.8452.

Species C. borleyi C. pictus L.fuelleborni P.genalutea C. borleyi 0.0000 C. pictus 7.0607 0.0000 L.fuelleborni 5.9251 9.9158 0.0000 P.genalutea 5.1429 7.8905 6.7377 0.0000 64 D.D. Kassamet al.

Figure 2. Thin-platespline deformation grids representing each species; (a) Copadiochromisborleyi ; (b) Ctenopharynxpictus ; (c) Labeotropheousfuelleborni ; (d) Petrotilapiagenalutea.

Table 2. Multiplecomparisons based on Tukey-Kramertest for two trophic characters. Right half represents comparisonsfor gape width, left half for interorbital width. Positive values denote signiŽ cantly differentpairs whereas negative values denote pairs that are not signiŽ cantly different.

Species C. borleyi C. pictus L.fuelleborni P.genalutea C. borleyi 0:914 3.659 4.586 ¡ C. pictus 1.521 3.933 4.859 L.fuelleborni 0.903 3.674 0:260 ¡ P.genalutea 1.468 4.238 0:685 ¡

SD; 8.3 2.7) than Ctenopharynxpictus (5:5 0:7).There was nodifference in gapewidth § between the twospecies ( Copadichromis§ borleyi ; 7:2 0:3 and Ctenopharynxpictus ; 6:9 0:3).There was also nosigniŽcant difference§ in either interobital widthor gape width § between the twoalgal feeders,but the means forthe twotrophic characters werehigher than those in zooplanktonfeeders (interorbital width, 10:5 1:4andgape width, 12 :1 0:3 for L.fuelleborni , while in P.genalutea , 11:1 1:5 and§ 12:9 0:3,respectively).§ The§shorter interorbital§ widthin the twozooplankton feeders might meanthat the orbit is larger,resulting inpossession oflarger eyes thanis the case foralgal feeders. As ana posteriori test, eyediameter was measuredand a signiŽcant difference was revealedamong species (ANOVA, F 101:9, P < 0:0001/.Subsequent pairwise comparisonsindicated signiŽcant differencesD betweenall pairs (Tukey- Kramertest, P < 0:05/ exceptthat of L.fuelleborni (6:7 0:5) and P.genalutea (7:2 0:6),whereas zooplankton feeders havelarger eyediameter § ( Copadichromis borleyi§ , 9:4 0:9 and Ctenopharynxpictus , 10:5 1:1). § § Therole of bodyshape in resource partitioning 65

Figure 3. Relationshipbetween body shape and trophic morphological characters using partial least squaresanalysis. Deformation grids are shown representing an individual towards the positive and negativeends of thebody shape axis. Individuals found on the positive side of the body shape axis correspondto algal feeders, while individuals found on the negative side of the body shape axis correspondto planktonfeeders.

Thetwo-block partial least squares analysis revealeda signiŽcant positive cor- relation betweenbody shape and the trophiccharacters ( r 0:779; P 0:001/, whichis shownin Žgure3. Individualstowards the positiveD endof the bodyD shape axis hada shorter butwider gape, a larger interorbital width,a short andnarrow head,a short butdeep caudal peduncle, and a deepmidbody. Specimens with this shapecorrespond to the twoalgal feeders.Individuals towards the negativeend of the bodyshape axis showthe oppositepattern andrepresent the twozooplankton feeders.They have a longerbut narrower gape and a shorter interorbital width.

DISCUSSION Alongstandingquestion in studies ofecomorphology is: doesmorphology relate totrophic ecology? Surprisingly ,this is notalways astraightforwardquestion to answer.In some cases, the relationship cannotbe made because differentiation introphic ecology does not always correspondto substantial variation in the trophicmorphology. In such cases, modulationof behavioural patterns maydrive the observeddifferences introphic ecology (e.g., Hori, 1983; Y uma,1994). Our results, however,provide some evidencelinking morphology and trophic ecology inthe species investigated. Usinglandmark-based morphometric methods, we foundsigniŽ cant differences in overall bodyshape. Furthermore, body shape 66 D.D. Kassamet al. variation was signiŽcantly correlated with gapewidth and interorbital width,two characters commonlyassociated withtrophic ability (Fryerand Iles, 1972).The most pronouncedvariation was foundin the headregion, particularly with respect togape size andgape position. This result implies that trophicmorphology has beenadapted to different feedingstrategies amongthese coexisting species. Such differential trophicmorphology helps toshed light onhow resources are partitioned, beit alongfood or spatial axes. Therelationship betweenfeeding habit andtrophic morphology of species within trophicguild appears consistent withecological specialisation. Inzooplankton feeders,for example, differences ingape size maybe related to feedingmicrohabitat partitioning. Copadichromis borleyi ,whichfeeds mainly fromthe water column, has asmaller gape,while Ctenopharynxpictus (a benthophagousfeeder) has alarger gape.This morphology-habitatassociation in the small-gaped,limnetic Copadichromisborleyi matches the classic description ofasuction feeder(Liem, 1991).By contrast, the larger gapeof Ctenopharynxpictus mayenable the Žsh to take large volumesof loose sediment into the mouth,from which the prey (mainly copepods)are sieved with longand numerous gill rakers (Ribbinket al., 1983).Thus, it appearsthat in LakeMalawi’ s zooplanktonfeeders, the classic benthic-limnetic nichepartitioning is seen withinthis trophicguild. Besides the gapesize, eyesize variation betweenthese twospecies seems toplay a vital role. Hart andGill (1994)reported that limnetic threespine stickleback havelarger orbits to accommodatea larger eye,which increases their resolvingpower for detecting small zooplanktonicprey .Wefound that these twozooplankton feeders, who have to detect tiny preyvisually (Fryerand Iles, 1972),also havelarger eyes,a result consistent with Žndingsin threespine stickleback. However, Ctenopharynxpictus beingbenthophagous, we hypothesise that searchingfor prey in sucha habitat requires ahigherresolving power, which is consistent with its larger eyes thanthose in its counterpart, Copadichromisborleyi . Inthe algal-feedingtrophic guild, segregation along a behaviouralaxis seems to playa signiŽcant role inmorphological divergence. Ribbink et al. (1983)reported that L.fuelleborni prefers foragingin shallow water,where the surgeis aprominent part ofthe environmentand where interspeciŽ c competitionis reduced.Its inferior subterminal mouth,a characteristic feature ofthis species, is usedto scrape algae fromrock surfaces while the bodyis orientedalmost parallel to the substrate (Fryer andIles, 1972;Ribbink et al., 1983;Albertson and Kocher, 2001). This foraging behaviouris contrasted with that of P.genalutea whichscrapes the rockswith its terminal mouthwhile its bodyis almost perpendicularto the substrate. Such subtle variation in foragingtechniques have been demonstrated to playa signiŽcant role inresource partitioning in otherguilds, such as epilithic algal-feedingand benthophagous-feedingcichlid species inLake T anganyika(see Yamaoka,1982, 1983,1991, 1997; Y uma,1994). The larger gapewidth revealed in the twoalgal feeders concordswith Fryer and Iles (1972)who stated that awidergape is Therole of bodyshape in resource partitioning 67 important foralgal feeding,as it enables the Žshto scrape awideband of rock surface at asingle application ofthe mouth. Barel’s (1983)observation that in most cases trophicgroups are morphologically identiŽed by particular ‘facies’(appearances) seems toconcur with ourŽ ndingsin the species examined.There appear to bemorphological features uniqueto each particular groupwhich are directly related to the preyconsumed, and how and wherethe preyis collected. Wesuggest that this variation incollection strategies, coupledwith trophicmorphological divergence, may enhance ecological separation, whichis probablya keyfactor leadingto coexistence throughreduced interspeciŽ c competition forresources. It canalso beargued that ecological separation followed bymorphological divergence may not only help in reducing competition among species, butmay also lead toecological speciation insympatry, which is oneof the proposedmodes of rapid speciation inAfrican cichlids (see Dieckmannand Doebeli,1999; Schluter, 1999; KornŽ eld andSmith, 2000). Theability to correlate trophicmorphology and trophic ecology using landmarks collected frombody shape shows the vital role whichbody shape plays in these cichlids. Inother Ž shes, bodyshape is functionallyrelated to feedingmode, where limnetic feeders are shallow bodiedwith longsnouts, and benthic feeders are deeper bodiedwith shorter snouts (Lavinand Mcphail, 1985; Caldecutt andAdams, 1998). This doesnot diminish the importanceof direct studies oftrophic structures, but rather complements them byproviding additional informationon the morphological variation within andbetween species. Further,by assessing the association between bodyshape and trophically important traits (e.g.,gape width), one may better understandthe morphologicaldiversity present in these amazinganimals. Ourstudy demonstrates that correlating bodyshape and trophic morphological characters allows usto gainknowledge of howcichlids capturetheir prey.Thus, an integrative approachaddressing both levels ofmorphological variation is the best wayof understandingthe diversity ofcichlid fauna.

Acknowledgement TheMalawi governmentthrough its Fisheries Departmentis acknowledgedfor allowingus tocollect samples fromLake Malawi. This research was sponsored in part byNational Science Foundationgrant DEB-0122281 (to DCA).

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