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Functional Significance of Variation in Trophic Morphology Within AnimalBiology ,Vol.54, No. 1, pp. 77-90 (2004) Ó KoninklijkeBrill NV ,Leiden,2004. Alsoavailable online - www.brill.nl Functional signicance of variation introphic morphology within feeding microhabitat-differentiated cichlidspecies inLake Malawi DAUD KASSAM 1; ,DEANC. ADAMS 2 andKOSAKU Y AMAOKA 1 1 Departmentof Aquaculture,Kochi University, B 200Monobe, Nankoku-shi, Kochi, 783-8502,Japan 2 Departmentof Ecology,Evolution and Organismal Biology, Iowa State University, Ames, Iowa50010, USA Abstract—Shapevariation in trophicmorphology between species in two trophic guilds (zooplankton andepilithic algal feeders) was investigated using landmark-based geometric morphometrics. Three disarticulatedbone elements from the head region were examined; the neurocranium, the premaxilla andlower jaw. From separate analyses of each bone element, signi cant shape variation was identi ed betweenspecies in each trophic guild. The deformation grids generated revealed that, for the zooplanktonfeeders, Ctenopharynxpictus hasa longerneurocranium, a longerand ventrally directed vomer,a largerorbit, a shorterascending arm, a shortermaxillad spine, and a morecompressed articularbone relative to Copadichromisborleyi .Inalgal feeders, Labeotropheusfuelleborni has ashorterneurocranium, a smallerorbit, a ventrallydirected vomer, a longerascending arm, a shorterdentigerous arm, increased height of the articular process, and a moreelongated dentary than Petrotilapiagenalutea .Observedanatomical differences are discussed in terms of function, specically with respect to thefeeding microhabitat differentiation between species in eachtrophic guild.These differences enable us to appreciate the role that trophic morphology plays in enhancing ecologicalsegregation, leading to coexistence of thespecies. Keywords:algalfeeders; Cichlidae; geometric morphometrics; thin-plate spline; zooplankton feed- ers INTRODUCTION Inthe East AfricanGreat Lakes,viz. Victoria, Tanganyikaand Malawi, many cichlid species are knownto coexist in highdensities alongthe rockyshores. Such coexistence is frequentlyattributed to the mannerin whichthese cichlids partition Correspondingauthor; e-mail: [email protected] 78 D.Kassam,D.C. Adams& K.Yamaoka resources throughtemporal, spatial andtrophic means (Ribbinket al., 1983;Witte, 1984;Bouton et al., 1997).Trophically, cichlids are knownto segregate along variousniche axes including:food size partitioning,quantitative differences in food composition,differences in foodcollecting strategies, andpartitioning of feeding microhabitats (Yamaoka,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, these trophically segregatedgroups can be identi ed by structural differences in their trophicmorphology ,eventhough such differentiation is related moreto the waythe foodis capturedand processed than to the typeof food consumed(Barel, 1983;Y amaoka,1997). The keyto trophicsegregation in cichlids appearsto bethe diversication ofthe oral jaw apparatusthat has enabledcichlids to evolvespecialised modesof feeding,and to utilise almost all available feeding niches. InLake Malawi, manycichlid species coexist alongthe rockyshores (e.g.,15 species at West Thumbiisland, ourcollection site; Ribbinket al., 1983).T oun- derstandfully whatmechanisms promotethe coexistence ofthese species, the role ofmorphologicalvariation within andbetween species must beinvestigated. Some studies havebegun to investigate this (e.g.Reinthal, 1989;Kassam et al., 2002a, b).Kassam et al. (2003a)examined the role ofbody shape in resourcepartitioning amongfour species coexisting alongLake Malawi’ s rockyshores: Copadichromis borleyi and Ctenopharynxpictus (zooplanktonfeeders), and Labeotropheusfuelle- borni and Petrotilapiagenalutea (epilithic algal feeders).These species are segre- gatedalong a foodaxis, andare segregatedspatially in terms offeedingmicrohab- itat. Ctenopharynxpictus is mainly benthophagous,but also feeds fromthe water columnwhen zooplankton is in abundance(T. Sato, pers. comm.), while its coun- terpart, Copadichromisborleyi, is reportedto feedfrom the openwater (Ribbinket al., 1983;Konings, 1990). The two algal feeders inhabit shallow rockyareas, but L.fuelleborni is commonlyfound on the sediment-free wave-beatensides ofthe rocks(Ribbink et al., 1983;Konings, 1990). Kassam et al. (2003a)found that the headregion was most morphologicallydivergent among these species. This nding promptedus to investigate furtherwhat speci c anatomical features maybe respon- sible forthe observedvariation in headshape. W etherefore,analysed several bone elements in the headregion: the neurocranium,the lowerjaw andthe premaxilla in the upperjaw. The neurocranium was includedbecause of the role it plays in conjunctionwith the oral jaws throughthe ethmovomerregion (Reinthal, 1989;Y a- maoka,1997; Albertson and Kocher, 2001). Thegoal of our study was to examinepatterns ofshape variation in these anatomical elements betweenspecies in eachtrophic guild, and determine whether the observedmorphological patterns relate to resourcepartitioning (especially feedingmicrohabitat differentiation), in anattempt to understandthe role that trophicmorphology plays as amechanism promotingspecies coexistence. Trophicmorphology of Malawian cichlids 79 MATERIALS AND METHODS Specimenpreparation Specimens (n 20per species) usedin this studywere collected fromW est ThumbiIsland as describedin Kassam et al. (2003a).The following species were used: Copadichromis borleyi (standardlength, SL, 80.5-127.5 mm), Ctenopharynx pictus (SL,78.6-101.3), L.fuelleborni (SL,81.7-104.2) and P.genalutea (SL, 85.9- 116.4).W eusedPotthoff ’s(1984)protocol to clear andstain all bonesin the headregion. Drawings of all anatomical structures weremade using a Leica-MS 5 microscopeattached to acamera lucida.These were later scannedand digitised for geometric morphometricanalysis. Osteological nomenclaturefollows that ofBarel et al. (1976). Geometric morphometricsand statistical analyses FollowingAlbertson and Kocher (2001), we focused on individual skeletal ele- ments, whichenables us to reveal patterns ofmorphologicalvariation that are other- wise obscuredif articulated skeletons orexternal morphologyalone is considered. Quantication ofthe shapeof eachdisarticulated bonestructure (neurocranium,pre- maxilla andlower jaw) was doneusing landmark-based geometric morphometrics (GM)methods (Rohlf and Marcus, 1993). First, TPSDIG32(Rohlf, 2001) was used to digitise the locations ofbiologically homologouslandmarks on the lateral side ofeachbone structure (g. 1). For the neurocranium,the followinglandmarks were recorded( g. 1a): 1)rostral tip ofthe vomer;2) caudal-most pointof the preorbital ridge; 3)dorsal tip ofthe suppraoccipital crest; 4)ventral process ofthe vertebrad concavity;5) pharyngobranchiad apophysis; 6) tip ofpostorbital process; 7)tip of preorbital process; 8)caudal-most pointof the vomerine-palatinadarticulation facet. Forthe premaxilla, velandmarks were recorded ( g. 1b):1) dorsal process ofthe ascendingspine; 2)rostro-most pointof the dentigerousarm; 3)caudalprocess of the dentigerousarm; 4)dorsal process ofthe maxillad spine; 5)ventro-mostpoint ofthe interprocess edge.Finally, eight landmarkswere recorded from the lowerjaw (g. 1c): 1)rostral tip ofthe dentary;2) dorsal tip ofthe coronoid(dentary) process; 3)dorsal tip ofthe primordial (articular) process; 4)dorsal process ofthe suspenso- riad articulation facet; 5)postarticulation process (ofthe suspensoriadarticulation facet); 6)retroarticular process; 7)rostral process ofthe coulter area; 8)tip ofthe rostral process ofthe articular. Theselandmarks were chosen for their capacity to represent prominentfeatures andto capturethe overall shapeand structure ofeach bone. Forall subsequentanalyses, the landmarkcoordinates from each bone were treated separately. First, all specimens weresuperimposed using the Generalised Procrustes Analysis (GPA)(Rohlfand Slice, 1990)to removenon-shape variation arising fromdifferences in scale, orientation andtranslation. Fromthe GPAaligned specimens, shapevariables wereobtained by generating partial warpscores and uniformcomponents using the thin-plate spline andstandard uniform equations 80 D.Kassam,D.C. Adams& K.Yamaoka Figure 1. Landmarkscollected on each skeletal element; a) neurocranium, b) premaxilla, c) lower jaw.The landmarks are de ned in Materialand Methods section. (Bookstein,1989, 1991, 1996). T ogether,the uniformand non-uniform components are treated as aset ofshapevariables forstatistical comparisonsof shape variation within andamong groups (see e.g.,Caldecutt andAdams, 1998; Adams and Rohlf, 2000;Rü ber and Adams, 2001; Kassam et al., 2003a,b). In addition to this analysis, the specimens foreach species weresuperimposed separately usingGP A,and the average(consensus) con guration of landmarks was obtained.These mean specimens werethen compared to the overall consensuscon guration (reference) to visualise shapevariation amongspecies usingthin-plate spline deformationgrids. TPSRELWsoftware (Rohlf,2002) was usedto performall these analyses. Toidentify anyshape variation amongspecies, aCanonicalV ariate Analysis (CVA)was performedon the weightmatrix ofshapevariables (partial warpscores anduniform components of shape).This analysis was performedseparately onthe shapedata foreach bone. When the multivariate analysis ofvariance (MANOV A) identied signi cant differences amongspecies, pairwise multiple comparisons usinggeneralised Mahalanobisdistance
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