Angiosperm Fleshy Fruits and Seed Dispersers: A Comparative Analysis of... Constraints in Plant-Animal Interactions

Angiosperm Fleshy Fruits and Seed Dispersers: A Comparative Analysis of Adaptation and Constraints in Plant-Animal Interactions Author(s): Pedro Jordano Reviewed work(s): Source: The American Naturalist, Vol. 145, No. 2 (Feb., 1995), pp. 163-191 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/2463122 . Accessed: 17/01/2012 11:49 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. The University of Chicago Press and The American Society of Naturalists are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org Vol. 145,No. 2 Naturalist The American February1995 ANGIOSPERM FLESHY FRUITS AND SEED DISPERSERS: A COMPARATIVE ANALYSIS OF ADAPTATION AND CONSTRAINTS IN PLANT-ANIMALINTERACTIONS PEDRO JORDANO* Estaci6nBiol6gicade Doniana,CSIC, Apdo. 1056,E-41080,Sevilla,Spain August24, 1993;RevisedMarch28, 1994;AcceptedMarch31, 1994 Submitted in phenotypic traitsofangiosperm fleshy fruits has beenexplainedas the Abstract.-Variation available By analyzing theinformation to theirmutualistic seeddispersers. resultofadaptations ofevolutionary species,I assessthehypothesis on fleshy of910angiosperm fruit characteristics traitsand typeof seed disperser(birds,mammals,and associationbetweenfruitphenotypic nullhypotheses about and quantitatively alternative mixeddispersers) and addressexplicitly affinity amongplanttaxa is accountedforby comparative phylogenetic effects.Phylogenetic contrasts. autocorrelation, and independent methodsincluding nestedANOVA, phylogenetic effects downto genuslevelexplain phylogenetic Averaging overthe 16 fruittraitsexamined, reaching are strong amongcloserelatives, autocorrelations 61% oftotalvariance.Phylogenetic contrast significance for 11 of the 16 fruittraitsexamined.Whenassessed by independent evolutionbetweentypeof disperserand fruittraitsis confinedto fruit methods,correlated for in othertraitsvanishafteraccounting amongdispersalsyndromes diameter.Differences arenotentirely interTheseanalysesrevealthatseeddispersalsyndromes effects. phylogenetic can be assessed to seed dispersers. Theirstatusas exaptations pretableas current adaptations studiesofnaturalselectionon fruitsize and rigorouscomparative by combining experimental hypotheses. and cladistictestsofadaptational Plantadaptationsto one or a fewseed dispersersare rarein nature,butrelasetsoffruit knownas syndromes (Ridley morphologies integrated tivelyinvariant, and interpreted as 1930; van der Pijl 1982;Janson1983)have been identified environment" (Howe reflecting broad adaptationsto the "disperser/dispersal is theasinterpretation 1986;Fleminget al. 1993).Centralto thisadaptationist is themain accruesto bothparts,and thisbenefit thata mutualbenefit sumption Recentstudieschallengethis thecoevolutionoftheinteraction. factorimpelling coevolution.Geneticconlimitations to plant-seed disperser viewbydiscovering andhistory straints (Herrera1986,1992a;Janson1992), (Howe 1984),phylogeny oftheinteractions (Jordano1987c),andextensivevariaandasymmetry diversity themselves(Howe 1983; Wheelwright tionin the outcomeof the interactions as the mainobstaclesfortheevolutionof tight,co1988)have been identified the A centralissue relevantto thisquestionis therefore evolvedrelationships. of "constraints"(McKitrick1993) and estimationof the relativemagnitudes mutualisms. "specificadaptations"in theevolutionofplant-frugivore *E-mail:jordano@cica.es. Am. Nat. 1995. Vol. 145, pp. 163-191. ? 1995 by The Universityof Chicago. 0003-0147/95/4502-0001$02.00. All rightsreserved. 164 THE AMERICANNATURALIST are important in Previousstudieshave suggested thatphylogenetic constraints plants(see, e.g., Lechowicz 1984;Hodgsonand Mackey 1986; Kochmerand Handel 1986;Herrera1987,1992b;Baldwinand Schultz1988;Michaelset al. 1988;Donoghue1989;Stratton1989;Willsonet al. 1989;Gorchov1990;Mazer 1990;Willsonand Whelan1990;Chazdon 1991; Lee et al. 1991; Schupp and Feener 1991;Bremerand Eriksson1992;Fischerand Chapman1993),butfew have attempted to considertheireffectsexplicitlyand quantitatively (but see Janson1992).A comparative approach(Pageland Harvey1988)is indispensable thatis attributable to commonancestry fromsimilarfordistinguishing similarity ityattributable to paralleland convergent evolutionary change.The latteris expected amongplantssharingthe same major seed dispersersif evolutionary traitsis attributable tocoevolvedselectivepressuresbyfrugivores. changeinfruit arenotnecessarily Notethatbothtypesofeffects mutually exclusive,as phylogetraitsbutset do notpreventnaturalselectionactingon phenotypic neticeffects a rigidpatternof covariationamongcharacters. limitsto itsactionby imposing A wholesetofrecently developedcomparative methods(Felsenstein1985;Pagel and Harvey1988,1989;Grafen1989;HarveyandPagel 1991;Harveyand Purvis 1991;MartinsandGarland1991;Garlandetal. 1992,1993)can be usedforassessingtheevolutionary associationamongquantitative charactersbut,as faras I know,haveneverbeenusedwithplantdata.HereI adoptan explicitly comparativeapproachto testforevolutionary associationsbetweenfruittraitsand seed disperser types. My objectivein thisarticleis to answerthefollowing questions.First,what fruits fraction oftotalphenotypic variancein angiosperm fleshy can be explained by sharedancestry?Residualvariationis likelythe resultof selectiveforces sensustricto) one ofthepoten(adaptations, (GouldandVrba1982)andcertainly tialmajorforcesis thatexertedbyfrugivores. Second,are fleshyfruitcharacternutrient in thepulppreisticssuch as fruitdesignand particular combinations dictablyassociatedwithseed dispersalby particularfrugivore groupswhen phylogenetic affinity amongplanttaxa is accountedfor?If phylogenetic affinity of totalphenotypic variancein fruittraits,we might explainsa largefraction forevolutionary modification offruitstructure as sugexpectsevereconstraints gestedby Herrera(1986,1992a)and Wheelwright (1988).Boththebroadset of plantdata consideredand thegeneralcategoriesof dispersertypesimposedby the availableinformation set limitations to thisanalysis.However,its validity stemsinidentifying generaltrends(androbustmethodsto assess them)thatbear on theimportant clade-wideassociationbetween questionof theevolutionary, fruitcharacters and seed dispersertypes. angiosperm fleshy ADAPTIVE HYPOTHESES AND PREDICTIONS The last two decadesof studieson thedispersalecologyof animal-dispersed plantshave centeredin adaptiveexplanationsof the enormousmorphological variationin fruittypesand frugivore behaviors(see reviewsin Howe 1986;Jordano 1992).A strictly statesthatfleshyfruitphenotypic adaptationist hypothesis variationis exclusivelytheresultof a plant'sadaptationto its seed dispersers PHYLOGENETICCONSTRAINTS IN FLESHY FRUITS 165 (Snow 1971;McKey 1975;Janson1983).The earliersurveysof Ridley(1930), Turcek(1961,1967),and van derPiji (1982),providing correlative evidencefor thehypothesis, have been largelysupported by moreexhaustivestudies(Snow 1981;Janson1983;Wheelwright et al. 1984;Gauthier-Hion et al. 1985;O'Dowd and Gill 1986;Debusscheet al. 1987;Herrera1987,1989;Debussche 1988;Debusscheand Isenmann1989;Willson1991,1993). Ideally,supportfortheadaptivehypothesis wouldcome fromdetailedmeasuresofnaturalselectionon fruit traitsin thefield.Bothexperimental studiesin captivity and fieldobservations have foundpositivecorrelations betweengape widthoffrugivorous birdsand maximum diameter ofthefruits ingested(Wheelwright 1985;Piper1986;Jordano1987b;DebusscheandIsenmann1989;Lambert 1989;also see Fleming1988),whichsuggeststhatindividual plantsmaydifferentiallydisperseseedson thebasisoffruit, seed size,or seed load variation(Howe and Vande Kerckhove1980,1981;Herrera1981,1984;Howe 1981;Piper1986; Jordano1987a;Obeso 1988;Wheelwright 1993;butsee Flemingetal. 1985;Foster 1990).Fieldevidencefordifferential fruit removalfromindividual cropsmediated in pulpnutrient by differences qualityis, however,scanty(Manasse and Howe 1983;Piper1986;Jordano1987a,1989;Herrera1988;Foster1990).In addition, mostofthesestudieshave shownthattheselectivepatterns by frugivores were whichaddedinconsistency in subjectto extremespatialand temporalvariation, theirstrength, and persistence. direction, inpreferandso forth, differ To theextentthatbirds,bats,nonflying mammals, fruit ence patterns fordifferent traits,theabove selectionpressuresmighttransstudiesacross late intothedifferences betweensyndromes foundin correlative can species (see Howe 1986,pp. 150-155;Fleminget al. 1993).The following thusbe predictedunderthepresence(or greatinfluence) of dispersal/disperser selectiveeffects: 1. Species in different disperser/dispersal categoriesshoulddifferin overall fruit morphology orparticular traitswhenphylogenetic effects are controlled for. after reductions Thevarianceexplainedbydisperser typewillnotshowsignificant withnonsignificant resultsfor forphylogenetic effects. controlling This,together methods(autocoreffects whenestimated phylogenetic byadequatecomparative will suggestthe absence of phylogenetic conrelation,independent contrasts), whichwouldadd supportto in fruitmorphology and pulpcomposition, straints theadaptivehypothesis. 2. Considera gradient ofvariationin thecomposition of thedisperserassemorpredominantly, blageamonga setofspecies,fromthosedispersedexclusively, of birdsand mammals by birds,throughthose showinga similarimportance (mixeddispersal),and then,at theotherextreme,thosedispersedexclusively, orpredominantly, bymammals.Ideallyeach specieswouldfallsomewhere along ofbirdsand mammalsin, say, thegradient on therelativeimportance depending number ofvisitsto theplants,totalfruit removal,or numberofestablishedseedthem. The adaptivehypothesispredicts from seed recruited lings dispersedby thatcan be summatrends of for fruit traits variation particular alongthisgradient relative of rizedas follows:overallfruit seed size, number, yield pulp,nonstructuand fiberwouldtendto increasefrom"bird" to "mixed" to ral carbohydrates, 166 THE AMERICANNATURALIST "mammal"dispersertypes.Individualseed size, energycontentper gramof pulp,lipids,and protein, wouldshowa decreasealongthisgradient. METHODS Data on traitsof angiosperm Quantitative information fleshyfruits(910 species in 392 generaand 94 families)was compiledfrombothpublishedand unpublished familieswiththisfruittype. sourcesincluding data on 42% of the angiosperm materialcomes fromcollections(C. M. Herreraand P. Jordano, Unpublished unpublished data)for42 speciesinCostaRica and severalMediterranean species not includedin Herrera'spublishedstudy(1987). The data include92 North American species,46 NorthEuropean,86 Mediterranean (Europe),277Neotropical, and409Paleotropical (244African,165Indo-Malayan-Australian). Copies of thedata set are availablefromme uponrequest(also see Jordano1992).Fruit size (lengthand diameter), freshfruitmass, drymass of seed(s) per fruit,dry individual seed drymass,numberof seeds perfruit,and massofpulpperfruit, relativecontentofdrypulpwithrespectto freshmassofthewholefruit(relative ofwater,proportions yield)wereconsidered"designtraits."Proportion oflipids, andacid-detergent fiberwithrespectto solublecarbohydrates, protein, minerals, drymass of pulp,as well as theenergycontentper gramof drymass of pulp, wereconsidered"nutrient content"traits.Figandthetotalenergycontent/fruit uresforrelativeyieldof pulp,totalenergyperfruit,and totalenergyper gram thesevariablesfromraw of pulpwerecomputedwhennecessaryforestimating data. theanalyticalmethodsused in thearticlessurveyedwereobviously Although varied,mostauthorsfollowedthemethodsoutlinedbytheAssociationofOfficial Chemists(1975).Lipidswereobtainedinmostcases withmicrosoxhlet Analytical content extraction andprotein bymicro-Kjeldahl analysis.Whenstudiesreported totalnitrogen (N), I used N x 6.25 as an estimateof crudeproteincontent. Studiesreporting analysesofthewholefruit (i.e., including seeds)wereexcluded. Ideally,each species shouldbe characterized of by the relativeproportions totalvisitsor fruitsremovedby each majorfrugivore group,correctedby their in termsof seedlingsrecruited effectiveness fromthe seeds removed(Murray is lackingformostspecies,and I 1988;Schupp1993).This typeof information to assignthemto threebroad categoriesalong a gradientbetween attempted speciestotally,or mostly,dispersedby birdsto speciestypicallydispersedby mammalsalone. Dispersertypecategoriesused as classificatory criteriawere dispersalpredominantly by birds,mixed(birdsand mammals),and mammals Previousstudieshaveemphasizeddifferences (primates, bats,ungulates). among thesebroadcategories(Ridley1930;Janson1983;Howe 1986;Fischerand Chapman1993),and I used themin theanalyses.These generalcategoriespose obvious limitations to thepresentanalysisbut,on theotherhand,solvethepotential finer"ad hoc" syndromes of establishing whenappropriate shortcomings informationis lackingformosttaxa(see table1 inFischerandChapman1993).Species wereassignedto thethreecategorieson thebasisofpublishedinformation inthe PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 167 originalarticles,generaltreatments (Ridley1930;Turcek1961,1967;Croat1978; van Roosmalen1985; Snowand Snow 1988;Willson1991,1993),personalcommentsoftheauthors,and personalobservations (C. M. Herreraand P. Jordano, unpublished data) forMediterranean and Europeanspecies and some Central Americantaxa. Assignments werebased mostlyon qualitativeassessmentsof thefrequency offeedingrecords,importance offruits in thediet,and frequency ofreferences withpositiverecordsoffeeding by different frugivore types.Informationaboutcongeneric speciestogether withfruit morphology (see Janson1983, 1992)was used in a fewcases. The robustness ofthesecriteriavariedobviously accordingwiththequalityofthebackground information we presently have for different plant-disperser systems.The categoriestherefore are rough,and future analysesmight showtheyhaveto be reassigned forsometaxa,butI am confident thatthegeneralconclusionsofthepresentanalysiswillhold.Thus,preliminary analyseswithdata subsetswithgreaterresolution ofdispersertypes(Mediterranean,NorthAmerican, andsomeNeotropical sets)didnotrevealthatpartitioning thedispersaltypesintoadditional categories(i.e., largeand smallbirds,batsand nonflying mammals)wouldalterthemainconclusions. Use of TaxonomicInformation I performed theanalysisusingtheclassification systemofCronquist(1981)and estimated effectsand relatedness phylogenetic usingthetaxonomicrelationship caveatmustbe madethat amongthe910 speciesin thedata set. The important a moreexplicitly is tobe preferred forfuture arrangement reanalyses phylogenetic informaofthisdataset.Morelocalanalyses,nowpossiblewiththephylogenetic thepowerofcomparationforcertaintaxa,havea greatpotential forincreasing tivetests(see, e.g., Erikssonand Bremer1991;Bremerand Eriksson1992)if combinedwithgreater ofthedisperser resolution types,andtheywillbe thegoal of subsequentarticles. A phylogenetic classification system(Sporne1956)is an estimateof a phylogButtheconcluenythatcan be usedto allowanalyseswithavailableinformation. sionsdrawnneedto be reassessedwhenmorerefined information phylogenetic becomesavailable.Miles and Dunham(1993)providean updateddiscussionof in comparative in choosinga well-supported the problemsinherent phylogeny when insteadof inherent taxonomies studiesand thepotential weaknesses using al. 1992). and Gauthier Garland et trees see de phylogenetic (also Querioz 1992; Statistical Analyses Nested ANOVA and autocorrelationmnethods.-Analyseswere performedon and angular variables(naturallogsforweightsandlineardimensions transformed The variancecomponents,as a percentage transformations forproportions). of totalvarianceforeach taxonomiclevel,wereestimatedwithNESTED and ofthe VARCOMPprocedures (SAS Institute 1988)and are used as a description and theirconsistency patternsofvariancepartitioning amongtraits.Taxonomic as nestedrandom andgenus)werespecified levels(class,subclass,order,family, effectswithineach higherlevel,withclass effectbeingfixed(Bell 1989).Howlevelsfortheseeffects,as thenominaldeever,I did notestimatesignificance 168 THE AMERICAN NATURALIST of the data, and the greesof freedomare lackingbecause of nonindependence nestedANOVA is heavilyunbalanced. autocorrelation method(Cheverudand Dow 1985;Cheverud The phylogenetic and Kot 1990)partitions thetotalphenotypic varianceof et al. 1985;Gittleman ofspeciesintoa component attributable to theirphylogea traitacrossa number inand a specificcomponent notattributable to phylogenetic neticrelationships coefficients and proportional varianceaccountedfor heritance.Autocorrelation wereestimated autocorrelation byphylogeny bya network model,y = p Wy + e, and Kot (1990). usingthemethoddescribedin detailby Gittleman theextentto whichthephenoautocorrelation The phylogenetic p, measuring thephylogeny, is estimatedby Wy, typictraitvalues (y) correlatethroughout in a traity amongspecies ofthetotalvariation representing a linearcombination or taxonomic relatedness weighedbytheirphylogenetic (matrixW). A maximum likelihoodprocedurewas used to estimatep and R2, thevarianceexplainedby themodel.Higherp valuesindicatethatthemorerelatedspeciestendto be more similar.I used Moran'sI statistic(Moran1950)to estimateautocorrelation; at traitofa specieswitha weighted anylevel,I comparedthephenotypic averageof The weights(wij)are functions ofthetaxonomic thetraitovera setofneighbors. relatedness ofthespeciesincludedin theanalysisto each other.I used a hierarchicaldistance(one forcongenericspecies,twoforconfamilial species,and so on up to fiveforspeciesin thesameclass). To improvemodelfitI used thegrid searchprocedurefora maximumlikelihoodestimatordescribedby Gittleman and Kot (1990)to derivewijvalues:wij= I1dU7,wheredijis thedistancebetween indexobtainedby maximum likelispeciesi andj, and a( is a variable-weighting function ofphylogehoodestimation. By thismethod,theformofthedecreasing values(wij)whenincreasing distanceneednotbe neticconnectivity phylogenetic assumeda priori,as intheCheverudet al. (1985)method.Alldatawerestandardized to meanzero and unitvariancepriorto the analysis.Residualsfromthe Gittleman and Kot modelweretestedforindependence autoregressive following (1990). Independentcontrastsmethods.-I addressed the hypothesisof functionalas- sociation(correlated and dispersalsyndrome evolution)betweenfruitcharacters contrasts methods(Felsenstein1985;Burt1989).I used the byusingindependent Contrasts(CAIC) package,version1.2, Comparative Analysisby Independent whichimplements a variety developedby A. Purvis(1991),OxfordUniversity, and discretevariables(Garlandet al. 1992).I report of methodsforcontinuous heretheresultsobtainedwiththepunctuational changeassumption (equal, fixed branchlengths),because analyseswiththe gradualisticassumption(variable consistent. The evolutionary branchlengths) werehighly correlation betweentwo charactersis testedby assessingthe relationship betweencontrastson the X variable(e.g.,disperser predictor type)andcontrasts on theY-dependent variable (e.g., fruitdiameter) (Harveyand Pagel 1991).If a positiverelationship between thetwotraitsexists,itwillshowup,whenthecontrasts are plotted,as a positive least squaresregression slope acrosstaxa. I testedthisrelationship by ordinary withcontrasts theorigin, standardized through usingbranchlengthsofthephyloI useda binomialtestto assess theprobability ofgetting genetictree.In addition, PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 169 an equal number ofpositiveandnegative ofpositivecontrasts; a givenproportion relationship beof no evolutionary contrasts are expectedunderthehypothesis tweenthetraitsexamined.HarveyandPagel(1991)andPageland Harvey(1992) and addresstheproblemofunregivedetailsforthecalculationofthecontrasts solvednodes,an issue forwhichthereis no optimalsolutionyet.The method nodesuses valuesoftheX variableto split at multiple usedto resolvepolytomies thetaxa (congeners)intotwogroups,above and belowthemeanofX, yielding is computedas thediffertwosubnodesforthemultiple node.The linearcontrast subnodes(Purvis1991). ence betweenvaluesoftheserecomputed I codeddispersertypeas a categoricalvariablewiththreelevels:birds,value the outputforthe of one; mixed,two; and mammals,three.I theninterpret traits(e.g., fruitdiameteror relationships betweencontrastson thecontinuous on thisvariableas a difference in proporlipidcontentofthepulp)and contrasts in the continuous tionsof each dispersercategoryassociatedwithdifferences trait.The rationaleforthisprocedurefollowslogicdevelopedby Fleminget al. ofdispersertypes (1993).Supposeeach speciesis locatedalongan idealgradient dispersedby birds, betweenan extremewithspeciestotally,or predominantly, dispersedby mammals. and anotherone withspeciestotally,or predominantly, Species withmixedseed dispersalwouldbe closerto one or theotherextreme depending on theirrelativerelianceon birdsand mammalsforfruitremovaland between,say, fruitsize seed dispersal.Thus, positiveand linearrelationships increasesin wouldmeanthatevolutionary contrasts and disperser typecontrasts of changesto a greaterproportion fruitsize are associatedwithevolutionary ofmammal be illustrated bya greaterproportion mammalian dispersalthatmight orbya greater coterieofthetaxainvolvedinthecontrast speciesinthedisperser ofseedsdispersedbymammals(PagelandHarvey1988;Harvey totalproportion and Pagel 1991). stated.Probaaregivenas meanand 1 SD, unlessotherwise Summary statistics bilitylevelswerefixedat .05. However,in mostinstancesI used a Bonferroniacrossgroupsare tablewise P level of .0031,sincemostcomparisons corrected testsforthe16fruittraitsconsideredhere(P = and involveseparateunivariate .05/16)(Rice 1989). RESULTS General Trendsof Variation A factoranalysis of the correlationmatrix(across species) between fruittraits revealsthatfivesignificant componentsaccountfor77.3% of totalvariation, amongtraits(table 1). Families patternof covariation whichindicatesa distinct ofspeciesvalueson thespace defined distributions showlargelynonoverlapping structure (fig.1), and familyeffectsaccountedfora 27.49% by thiscomponent of totalvariationon principalcomponent(PC) 1 and 8.48% forPC 2. Note tests(ANOVA, MANOVA) forthesedifferences thatconventional parametric becausespeciesare estimates, wouldyieldinvalidP valuesandbiasedparameter not phylogenetically independent,and the nominaldegrees of freedomwould be 170 THE AMERICAN NATURALIST TABLE 1 RESULTS OF A FACTOR ANALYSIS OF ANGIOSPERM FLESHY FRUIT TRAITS BASED ON THE CORRELATION MATRICES OF BOTH ORIGINAL VARIABLES AND INDEPENDENT CONTRASTS FruitTrait Fruitlength Fruitdiameter Fruitfreshmass Pulp drymass Seed(s) drymass/fruit Numberof seeds/fruit Seed drymass Relative yield of pulp Energycontent/gpulp PC I .4227 .8952 .4110 .8506 .4379 .9320 .4018 .8776 .3662 .8043 . . . . ... . . . .4554 . . . * . . ... PC 2 PC 3 ... . . . ... ... . . . ... . . . ... . . . . . . . . . . . . . .. . . . . . . . . . . . . -.2983 Water in pulp (%) .3619 .8764 ... .7603 . . . . . . . . Lipids . . . . .. . . . .2674 . .. . . . Energycontent/fruit Protein Nonstructuralcarbohydrates Minerals Fiber Eigenvalues % Variance * . . . . . ... . . . . . . ... 5.31 4.93 33.22 30.83 - .8118 .8216 . . . .3747 ... 2.74 2.20 17.11 13.75 PC 4 ... .... . .. .. . . ... .... . . . . .. .. ... .... . .. .. ... .. . .. ... . . . ... . . . . . . . . . . . . . .. . . . . . . .5878 .6608 . . . . . . .2581 .3223 -.4858 -.7645 . . . . . ... . . .. ... .9170 . . . -.7066 ... ... . .. . . . . .. . . ... . . .. . . . . .. - .6427 . . . . . . . .. . . . .4571 .5968 1.61 1.71 10.09 10.66 PC 5 . . . . . . . .7328 .. . -.6140 .3024 - .3888 ... .4579 ... .8710 .... - .6088 - .3563 ... 1.41 1.56 8.82 9.77 1.29 1.20 8.05 7.49 NOTE.-Varimax rotationmethodwithprincipalcomponentextractionwas used on both the correlationmatrixforall species in the sample withpairwisedeletionof missingvalues (originalvariables, values not in italic) and the correlationmatrixfor independentcontrastsin each variable (values in italic). Figures show correlationsof each variable witheach principalcomponent(PC 1-PC 5). Only these fivecomponents,witheigenvalues >1.0, were considered significant (Legendre and Legendre 1979). Loadings < 10.251are omitted. I repeatedtheprincipal incorrect. components analysis(PCA) on the Therefore, matrix correlation obtainedfortheindependent contrasts. Resultswerehighly consistentwiththepattern obtainedfromthepreviousanalysis(table1), as expected fromthesignificant consistencybetweenthetwo matrices(r = 0.8057, t = 7.24, P < .0001;Manteltestwithrandomization, n = 1,000)(LegendreandLegendre1979). Because of the strongcovariationamongall size variables,taxa witheither PHYLOGENETIC CONSTRAINTS IN FLESHY 2- FRUITS 171 Lauraceae ,1/~~~~~~~~~~~~~Sml'lacaceae 1 Viscaceae 0 Ericaceae Rosaceae Ebenaceae -12- myrtaceae \ Caprifoliaceae ----- oraceae Oleaceae - -- - - - --- ---- 2Pa/mae Celastraceae ,acourtiaceae Rhamnaceae Palmae 0 AnacardiaceaeRuica racea ubiaceae Rutaceae Sapotaceae Rhamnaceae flacourtiaceae m O AralilveaemsolanDC@aE 1 ;Mliacea 2Myristicaceae ci ~ ~ -1 ibr hw 0ipid cotetan for . oftoAraliaceae y C f -2 -1 P Solanaceae Liliaceae -3 Vitaceae ~ihostvelado ~ ~ 0 1 2 3 Verbenaceae C,annntrcurlaboyraeCucurbitaceae e MelastoV (ceae -3 PC 1 -2 -1 0 1 2 3 FIG. 1.-Relative locationsofangiosperm twoprincipal on thefirst species,byfamilies, offleshy fruitcharacteristics. components ellipses(P = .900)are plotted Equal frequency foreach family. These ellipsesare thecontourlinesencompassing 90% of thedata points Fruit-size-related variableshavehighpositiveloadson PC 1, both (species)foreachfamily. lipidcontentand fibershowhighpositiveloads on PC 2, and nonstructural carbohydrates and energycontent pergramofpulphavenegativeloadson it(table1). Bothaxes account for50.3%oftotalvariance. fruits(e.g., Moraceae) or large,drupaceous,or few-seeded large,multiseeded fruits(e.g., Lauraceae,Rutaceae,Sapotaceae,someRosaceae) scorehighon a associatedwithoverallfruitsize (fig.1). Small-fruited first taxa,notacomponent bly Caprifoliaceae(Sambucus), Loranthaceae(Cladocolea), Viscaceae (Dendrophtora), Thymelaeaceae(Daphne), Melastomataceae(Miconia), and some Rubiaceae(Nertera,Putoria,Relbunium) scorelow on it. Onlythefirstand fifth 172 THE AMERICAN NATURALIST whichdepictthetrade-off betweenindividualseed mass and seed components, numberperfruit, involvelargeloads of"morphological" traits.The components 2, 3, and4 involvepulp"nutritional" traits(table1). Thus,PC 2 is interpretable Taxa betweenlipidsand nonstructural bythestrongdissociation carbohydrates. withlipid-rich and relatively fibrouspulp score highon it (mostPalmae, Lauraceae, Myristicaceae, some Anacardiaceae,and Celastraceae).Fruitsrichin soluble carbohydrates,such as Mimusops, Sideroxylon(Sapotaceae), Pancovia, Paullinia (Sapindaceae), Dictyophleba, Lacmellea (Apocynaceae), and most andCapriMelastomataceae, Rhamnaceae, Flacourtiaceae, Rosaceae,Myrtaceae, foliaceaeshownegativescoreson PC 2 (fig.1). theinverserelationship across species The thirdcomponent (PC 3) illustrates betweenrelativeyieldof pulp,energycontentperfruitand fiber,on one hand, and pulp watercontenton the other(table 1). The watery,succulentfruitsof Liliaceae (Clintonia,Dianella, Paris), Ranunculaceae (Actaea), some Rubiaceae (Coprosma, Coussarea), and Empetraceae (Empetrum)species score negatively richinminerals.Taxa with on thisaxis. These specieshaverelatively largefruits relatively dry,fibrous, and pulpyfruitstypically yielda highamountof energy and show highpositive of themajororganiccomponent, per fruit,irrespective scores on this PC 3; they include Crataegus, Hesperomeles, Sorbus and Pyrus (Rosaceae), Arbutusand Arctostaphylos(Ericaceae), Elaeocarpus and Muntingia (Elaeocarpaceae),Ziziphus(Rhamnaceae),and someAnnonaceae. Finally,specieswithhighproteinand mineralcontentsshownegativescores on PC 4 (EkebergiaandsomeTrichilia, Meliaceae;Ximenia,Olacaceae; Zingibershowhighcontent aceae, and mostPiperaceae).In addition,taxa thattypically inthepulpscorenegatively on thisaxis,andtheseinclude ofnonprotein nitrogen Ruscus, Ripogonum (Liliaceae); Bryonia, Citrullus,Coccinia (Cucurbitaceae); Tamus(Dioscoreaceae);and Mandragora(Solanaceae). Phylogeneticand AdaptiveEffectsin FruitPhenotypicVariance Phylogenetic variance components.-Partitioning of phenotypic variation amonghighercategoriesintheLinneanhierarchy (fig.2) suggestshighsimilarity in fruittraitsamongclose phylogenetic relatives.On theaverage,phylogenetic effects downto genuslevelexplain61% oftotalphenotypic varianceinthetraits examined.All thetestsrevealedlargeeffects ofthenestedtaxonomichierarchy on the16fruit from26.1% (relativeyield traits,withexplainedvariancesranging of pulp)to 89.2% (numberof seeds per fruit).For 13 of 16 traits,the variance explainedby thenestedmodelaccountedformorethan30.0% oftotalvariance. The intraclasscorrelation less coefficients up to theordinallevelweregenerally than0.15, whichindicatesthata negligible fractionof totalvariancewas acinthissample.Onlyseed(s) dry countedforbyclass, subclass,and ordereffects individualseed drymass,and mineralsshowedrelatively largesubmass/fruit, class and ordereffects,withintraclasscorrelationsbetween0.20 and 0.30 (fig.2). were large for most formand designtraits Familyintraclasscorrelations (fig.2), especiallyfruit, pulp,and seed(s)masses,individual seed mass,and seed numberper fruit.This patterncontrastswiththe smallerfamilialeffectsand PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS M Class 1 Subclass M Order M Family E 173 Genus FWithin genus 100 (D < LI Q / 0 Formanddesign Fruit trait Nutrient content levels(class to FIG. 2.-Percentagesof totaltraitvarianceaccountedforby taxonomic classification systemin a nestedANOVA ofangiogenus)ofCronquist (1981)phylogenetic Fruittraits aregrouped in"formanddesign,"orstructural, spermfleshy fruit characteristics. length;DIAM, andnutrient content characteristics. Abbreviations fortraitsareLENG, fruit fruit diameter; FRFM,fruit freshmass;PDM, pulpdrymass;8DM, drymassofseed(s)per RY, relative fruit;SEEDM, drymassofindividual seed; SEEDS, number ofseedsperfruit; yieldof pulp(100 PDM/FRFM);PCW,percentage watercontent;KJFR,energycontent contentsare givenas (kJ)per fruit;KJG,energycontentpergramof drypulp.Nutrient proportions relativeto pulpdrymass:LIP, lipids;PRO, protein; NSC, nonstructural carbohydrates; ASH, minerals; FIB, fiber. greatergenericeffectsexhibitedby nutrient traits(fig.2). Excludingthe conforfamily structed variatesRY, KJFR,and KJG,averageintraclasscorrelations higherthanthosefornutriamongformand designtraits(0.459)are significantly all taxonomiclevelsdown entcontenttraits(0.209;t = 2.27, P = .04). Including to genus,the differences betweenthe two groupsof traitsare onlymarginally forgenus,0.697 and 0.523, respecsignificant (averageintraclasscorrelations thetwogroupsoftraitsdiffer inthetypes tively;t = 1.77,P = .105).Therefore, of phylogenetic effectsbut onlymarginally in the overallmagnitudeof these effects. Phylogenetic and specificcomponents:an autocorrelationmodel.-By fitting theautoregressive model,significant autocorrelations wereobtainedfor11ofthe on 16fruittraitsexamined(table2). Thisindicatesa generaleffectofphylogeny As estimated byR2,sizable mostphenotypic variation ofangiosperm fleshy fruits. significant fractions of totalvariancein fruitand seed masses,fruitseediness, (taenergyreward/fruit, and lipidcontentcan be accountedforby phylogeny showsignificant ble2). Fruitdimensions, pulpwatercontent, andprotein phyloge- 174 THE AMERICAN NATURALIST TABLE 2 PHYLOGENETIC AUTOCORRELATION COEFFICIENTS (p), ASSOCIATED SE, R2, ANDSAMPLESIZE, FOR ANGIOSPERM FLESHYFRUITTRAITS FruitTrait Fruitlength Fruitdiameter Fruitfreshmass Pulp drymass Seed(s) drymass/fruit Number of seeds/fruit Seed drymass Relative yield of pulp Energycontent/gpulp Energycontent/fruit Water in pulp (%) Lipids Protein Nonstructuralcarbohydrates Minerals Fiber n 504 597 428 376 263 320 194 370 453 233 506 495 561 462 264 232 a 1.00 3.30 1.00 1.40 1.00 1.30 3.00 7.00 .10 1.10 4.00 1.20 8.00 .001 .20 7.00 p P SE(r) R2 .24 .24 .46 .42 .38 .34 .44 .10 .16 .37 .21 .41 .14 .15 .06 .03 * * * * * * * .043 .043 .041 .045 .055 .051 .059 .052 .046 .058 .043 .039 .042 .046 .062 .066 7.65 8.29 29.68 25.67 21.76 16.80 31.56 2.16 3.46 21.67 7.12 23.12 4.03 3.04 .55 .14 NS NS * * * * NS NS NS Coefficienta is a NOTE.-Variable n, numberof species; P, probabilitylevel; NS, nonsignificant. maximumlikelihoodestimateof the variable weightingindex used to obtain phylogeneticdistances (see text); R2 is the totalamountof variation(%) explained by the phylogeny.Asterisksmarksignificant values forthe Bonferroni-corrected probabilitylevel P < .05/16 = .003. neticcomponents, buttheseaccountformuchlowerfractions oftotalphenotypic variance.Finally,relativeyieldof pulp,mass-specific energycontent,soluble and fibershownegligible effects(table2). carbohydrates, minerals, phylogenetic forfruit traitscomputedaccording Figure3 showsthetaxonomic correlograms to Gittleman and Kot (1990).These values of Moran'sI depictthecorrelations betweentraitvaluesandweighted averagesofthesevaluesoversetsoftaxonomic neighbors. The correlograms locate wherethetaxonomiceffectsshow up and, if the way phylogenetic autocorrelations moreimportantly, changewithtaxonomicdistanceis consistent acrosstraits.A patternthatemergesfromfigure3 withstrongautocorrelations is thatmostfruit traitsshowdecayingcorrelograms, betweenclose taxonomic relativesthatdecreasewhenone proceedsup theLinnean hierarchy. The decayingof I values is steeperfordesigntraitsthanfor nutrient traits,whichadds supportto the resultsreportedabove fromnested ANOVA. EvolutionaryAssociations betweenFruitPhenotypicVariationand Type of Seed Disperser Patterns of variation associated with seed dispersal syndromes.-A central issue in thisstudyis whether differences betweenseed dispersalsyndromes are betweenspecies are controlled supportedwhenthe phylogenetic relationships for.To an unknowndegree,thesedifferences mayarise fromthe association between phylogenyand fruitcharacteristics,because individualspecies are not datapoints. independent CONSTRAINTS IN FLESHY PHYLOGENETIC FRUITS 175 Nutrients Design * LENG +DIAM A FRFM T PDM * SDM ESEEDS XSEEDM D RY * KJG + KJFR A PCW T LIP * PRO * NSC X ASH U FIB 0.8 0.6 0.2 -0.2 -0.4 GEN FAM ORD SCL CL GEN FAM ORD SCL CL Taxonomiclevel fordesignand nutrient FIG. 3.-Phylogenetic contenttraits(abbreviations correlograms as in fig.2) of angiosperm fleshyfruits.Values of Moran'sI statisticat variousnested order,subclass,and class,alongtheabscissa)are plotted taxonomic levels(genus,family, I values('max)forcomparison foreachfruit trait.Moran'sI valueswererescaledbymaximum correlations showhow phylogenetic and Kot 1990).Correlograms acrosstraits(Gittleman hierarchy. changealongthenestedtaxonomic are consumedand seeds specieswhosefruits similarity, Ignoring phylogenetic differin mostfruittraits frugivores typesof vertebrate dispersedby different observableconfirm examined(tables3 and4), andthegeneraltrendsofvariation thosefoundin previousstudieswithsmallerdata sets. First,averagefruitsize, increasesfrom eitherbythelength, diameter, orfreshmassofthefruit, estimated valuesfor species,withintermediate speciesto mammal-dispersed bird-dispersed taxa withmixeddispersal.Second,thetotalenergyrewardper fruitincreases, ina paralleltrend,frombird-to mammal-dispersed species,a resultofthestrong size anddrymassofpulpperfruit. Third, correlation acrossspeciesbetweenfruit energycontentsthan speciesshowhigherlipidand mass-specific bird-dispersed species. mixed-and mammal-dispersed Controllingphylogeneticvariation.-Comparisons across species in fruittraits associationsbetweentraitvalues have beenroutinely used to inferevolutionary in table3, and is illustrated and typeofseed disperser.Thistypeofcomparison thestatistical of theANOVA testsamongseed dispersergroupsis significance intypeofseed disperserdiffer intable4. Groupsofspeciesdiffering summarized in nineofthe16fruit accounts traitsexamined.However,thiseffect significantly forless than20% ofvarianceofanytrait(table4). affinities among If thesedifferences are mainlytheresultof thephylogenetic forthe influenceof shared species,thentheywould vanishwhencontrolling 176 THE AMERICAN NATURALIST TABLE 3 SUMMARY STATISTICS FOR FRUIT TRAITS OF ANGIOSPERM SPECIES DISPERSED VERTEBRATE FRUGIVORES BIRDS FRUIT TRAIT Fruit length Fruit diameter MIXED* Mean SD n Mean 11.88 7.22 266 14.70 10.21 5.37 Fruitfreshmass 1.485 4.792 Pulp drymass .144 .303 .406 Seed(s) drymass/fruit .185 Numberof seeds/fruit 8.9 32.5 Seed drymass 0.1097 .4753 Relative yield of pulp 13.65 6.84 Energy content/g pulp Energy content/fruit Water in pulp (%) Lipids Protein Nonstructural carbohydrates Minerals Fiber BY DIFFERENT 332 13.20 SD 7.96 MAMMALS n Mean 192 29.28 7.32 217 23.56 5.56 173 14.64 221 15.38 71.82 .149 .063 16.02 .171 .046 259 228 264 73.57 .070 .057 14.46 .125 .041 203 207 231 72.29 .082 .051 .540 .055 .130 .270 .038 .099 204 121 98 .565 .047 .170 .273 .028 .110 197 .597 .047 .150 2.18 4.49 SD n 22.75 46 18.56 48 264 1.881 3.469 134 5.611 15.898 .274 .465 119 .637 .842 238 172 .163 .227 76 .310 .428 203 106.9 494.1 93 8.3 20.1 .5532 14.738 123 .0803 .1655 58 8.70 234 16.68 117 20.04 12.05 5.70 17.87 TYPES OF 159 4.02 6.04 63 16.99 111 103 5.13 16.35 30 19 15 24 13 19 59 11 16.30 44 .138 60 .035 66 .251 61 .036 32 .127 31 masses in grams,energycontentsin kilojoules, and values NOTE.-Lengths are givenin millimeters for lipids to fiber are proportions relative to dry mass of pulp. * Seeds dispersed by birds and mammals. In thissituation, I wouldalso expectlargereductions inR2valueswhen ancestry. It is possibleto perform effects are subtracted. suchtestswiththe phylogenetic thedifferences betweendispersalsyndromes on autoregressive model,bytesting thespecificvalues,S, whichrepresent residualvariation.The mainassumption is thatthisresidualdepictstheindependent evolutionofeach species.Thus, S = T - pWy, whereT is thetotalphenotypic value,represented bythey vector(Cheverudand Dow 1985;Cheverudet al. 1985).I rantheANOVA testsforeach traitagainon theseS valuesin orderto testfordifferences betweenseed dispersertypescontrolling forphylogenetic effects.Table 4 showsthatthe numberof traitswith differences significant decreasedfromnineto six. In addition,R2 values were reduced,on the average,32% of the initialvalues explainedwhenusingtotal phenotypic variation. Traitsstillshowingsignificant betweentypesof differences seed disperserwhencontrolling forphylogenetic effectswere fruitlengthand diameter, fruitand pulpmasses,energycontent/fruit, and lipids.The variance accountedforby thismodelwas extremely low forlipids(4.8%), freshfruit mass (3.2%), and pulp drymass (6.8%), whichindicatesthatsizable variation attributable to majorseed dispersers is reallypresentonlyin fruitsize and total content/fruit energetic (largelya correlateoffruitsize). PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 177 TABLE 4 SIGNIFICANCEOF THE DIFFERENCESIN FRUIT TRAITS AMONGSPECIES PREDOMINANTLYDISPERSED BY BIRDS (B), MAMMALS(Mm-BATS, UNGULATES,PRIMATES),AND WITH MIXED SEED DISPERSAL BY BOTH GROUPS OF FRUGIVOROUSVERTEBRATES(Mx) TOTAL PHENOTYPIC VARIATION FRUIT TRAITS (df) Fruitlength(2, 503) Fruitdiameter(2, 596) Fruitfreshmass (2, 429) Relative yield of pulp (2, 371) Pulp drymass (2, 377) Seed(s) drymass/fruit (2, 264) Number of seeds/fruit (2, 322) Seed drymass (2, 193) Energycontent/gpulp (2, 455) Energycontent/fruit (2, 234) Water in pulp (%) (2, 508) Lipids (2, 497) Protein(2, 563) Nonstructuralcarbohydrates (2, 464) Minerals (2, 263) Fiber (2, 231) PHYLOGENETICVARIATION CONTROLLED F R2 B Mx Mm 44.61* 49.61* 19.83* 6.94* 25.18* 15.1 14.3 8.5 3.6 11.9 2.7 5.2 2.0 4.6 19.4 .2 7.9 .9 A A A A A A A A A A A A A B B B B B A B A B B A B A C C C B B A A A AB C A B A .5 A 1.3 A 3.39NS 2.9 A A A B A A B 3.63NS 8.7 1* 1.98NS 10.80* 27.67* .62NS 21.16* 2.62NS 1.13NS 1.76NS F R2 B Mx Mm 1.33NS A B A B A AB A B A B A A A A A A A B A A .1 A A 4.8 A B .5 A A 1.36NS 2.22NS 3.14NS .6 A 1.7 A 2.7 A 13.6 12.3 3.2 6.98NS 2.6 4.94Ns 13.67* 6.8 2.1 2.77NS 1.4 2.35NS 1.1 1.06NS 6.91NS 2.9 19.83* 14.6 39.33* 41.40* .33NS 12.62* A A A C C B AB B A A A AB B A B A A A A NOTE.-Separate ANOVA tests were carriedout on the total phenotypicvariance and on residual variance aftercontrollingforphylogeneticeffectsby means of an autocorrelationmethod(see text). R2 is the percentageof variationexplainedby the model (dispersercategories). Entrieswithdifferent lettersindicate significant differences(Scheffea posterioritest,P < .05) between the means of each traitvariable. NS, Not significant. * P < .003, Bonferroni-corrected significancelevel (P = .05/16 = .003). Independent contrastsanalysis.-The angiosperm classification phylogenetic of Cronquist(1981)providesa totalof 541 nodesforthe910 speciesin thedata witha bifurcating of set, 59.5% of themaximum possibleresolution phylogeny 909 nodes.The numberofnodesavailablefora giventraitis reduced,however, valuesandbythefactthatvariation fortypeofseed disperser becauseofmissing is absentat a numberof nodes (contrastswithvalue zero), especiallygeneric nodes.Mostcongenerssharethesametypeofseed dispersalagent,as expected fruitmorphology and pulpcomposition by theconservative shownat thistaxonomiclevel(fig.2). theresultsofbothregression theoriginand sign Table 5 summarizes through and thelatterare plottedin figure4. Each testson thecontrastscomparisons, ofthetypeof seed disindicatesan independent pointin thisfigure comparison in the in traitvalue a taxon perser given plottedagainst independent comparison forthattaxon.Contrastsin typeof seed disperser(independent variable)are as an forcedto be positive,and theirvalues alongtheX-axisare interpretable in of mammals the of each taxon increasing importance dispersal (see Methods). 178 THE AMERICAN NATURALIST TABLE 5 SUMMARY OF THEANALYSIS OF THERELATIONSHIPS BETWEEN DISPERSER-TYPE CONTRASTS ANDFRUIT TRAITCONTRASTS FORANGIOSPERM SPECIES NUMBEROF CONTRASTS FRUITTRAIT df SLOPE Positive Negative Fruitlength Fruitdiameter Fruitfreshmass Pulp drymass Seed(s) drymass/fruit Seed drymass Numberof seeds/fruit Relative yield of pulp Energycontent/fruit Energycontent/gpulp Water in pulp (%) Lipids Protein Nonstructuralcarbohydrates Minerals Fiber 164 183 50 138 104 83 114 137 100 154 165 163 174 157 114 99 .1278* .1183* 92 107 86 73 60 47 35 73 59 68 84 68 92 85 54 45 67 71 64 65 42 35 38 64 41 86 80 95 78 71 55 49 .2145NS .3124* 136INS .3144NS - 9248NS 0545NS .3553* -.0464NS .0348NS - .0727* -.0124NS - .0207NS 0162NS 0019NS BINOMIAL P .075 .01 NS NS NS NS NS NS NS NS NS .10 NS NS NS NS NOTE.-For each trait,separate regressionsthroughthe originwere calculated between dispersertype contrastsand fruittraitcontrasts.NS, Not significant.Bonferroni-corrected significancelevels are given forslopes. Binomialprobabilitiesare the P levels forthe binomialtest on an equal number of positiveand negativecontrastsforeach trait.Constrastsequal to zero forthe typeof seed disperser were excluded fromcalculationof the regressionslopes and binomialP. * P < .05/16 = .0031. I omittedthosetaxa thatwereinternally homogeneouswithregardto typeof seed disperser.Independent contrastsforthe traitvalues (Y variable)can be indicates zero,positive,or negative.Each pairofpositiveX-Y valuestherefore an independent instancein whicha changeformixedor mammal evolutionary dispersal(i.e., an increasein therelativeimportance of mammalsas dispersers ofa taxon)has beenassociatedwitha positivechangein thetraitvalue (i.e., an increasein fruitor seed size, pulpmass,or amountof a givennutrient). withthose Resultsoftheindependent contrasts analyses(table5) areconsistent methods(table4). The prevailing obtainedusingtheautoregressive illuspattern 4 is thatevolutionary and typeof tratedbyfigure changesinfruitcharacteristics seed disperser havebeenlargelyindependent. formand designvariAmongfruit anddrymassofpulpshoweda significant trend ablesonlyfruit length, diameter, of syndromes(fig.4A). to increasealong the bird-mixed-mammal continuum Amongnutrient contenttraits,onlyenergycontentper fruitand lipidcontent showedsignificant trends(table 5; fig.4B), but the correlation forlipidswas negative.The correlation of energycontent/fruit is a side effectof the strong covariation betweenthisderivedvariableandfruitsize. Obviously,largerfruits, witha greateramountof pulp,also yielda greateramountof energyper fruit. betweendisperser andenergycontent/ Thus,thepartialcorrelation typecontrasts fruitcontrasts is only0.001afterfruitsize effects are removed(bypartialing out PHYLOGENETICCONSTRAINTS IN FLESHY FRUITS 179 fruitdiameter).Therefore, theonlyevolutionary correlations evidencedby the independent contrastanalysisinvolvefruitsize and lipidcontent. The negativecorrelation betweenlipidcontentcontrastsand dispersertype contrasts (table5; fig.4B) indicatesthathighlipidcontentis evolutionarily associatedwithavianseed dispersalanddecreasesamongtaxawithmammaldispersal. However,R' is verysmallforthistrait(5.6%),andthecorrelation vanisheswhen controlling the influence of threeoutliers(thethreebottomdata pointsin the panelforlipids,fig.4B). These contrasts correspond to thegenusAglaia (Meliaceae), andfamilies AnacardiaceaeandApocynaceae,whichshowrelatively large amountsoflipidsin thepulpbutwithextremevariationamongspeciesdiffering indisperser type.AmongApocynaceae,specieswithmixeddispersalshowmuch higherlipidcontent(0.34 + 0.09, n = 3; generaStemmadeniaand Tabernaemontana) thanthose dispersedby mammals(e.g., genera Lacmellea, Thevetia,Landolphia; 0.044 + 0.063, n = 6). The same trendoccurs in Anacardiaceae, where bird-dispersed Pistacia, Rhus, and Harpehyllum show averageproportions of lipids(0.378 + 0.07,n = 6) wellabove specieswithmixeddisperserssuchas in genera Spondias, Pseudospondias, Tapirira, Trichoscypha, and Sclerocarya (0.025 + 0.07, n = 6). Finally,the same extremetrendexistsamongAglaia, withlipidcontentof0.492 + 0.09,n = 3, in bird-and mixed-dispersed taxa and 0.089 + 0.059,n = 3, amongmammal-dispersed species. As indicatedby the binomialtests(table5), thereis evidenceonlyfortaxa withgreaterproportions of mammal-dispersed speciesto showlargerfruits;the forfruitlength. signtestsare significant onlyforfruitdiameterand, marginally, The resultstherefore indicatethatcorrelatedevolutionbetweentypeof seed is largelyconfinedto fruit characteristics disperserand fleshyfruitphenotypic size, especiallytheexternaldimensions. Pairwise comparisonsamong congeners.-I carriedout a furthertest to see if thetrendsshownin tables4 and 5 andfigure 4 holdwhencloselyrelatedspecies in typeof seed disperserare compared.I selectedthosegenerain the differing intypeofseeddisperser.For each genus, datasetforwhichseveralspeciesdiffer I averagedtraitvalues across species sharingthe typeof seed disperserand comparedthesemeansamongdisperser categories(Wanntorp 1983).I talliedthe numberof generashowingincreasesor decreasesin averagetraitvalues when congenersdispersedby birdsare comparedwiththosedispersedby birdsand mammals(mixeddispersal)and/orthosethatare mammaldispersed.Each comto a signtestunderthe observation parisonwithina genusadds an independent nullhypothesis shouldgo in the thatequal numberofwithin-genus comparisons samedirection. trendforlarger The pairwisecomparisons(table6) revealonlya significant fruits(greaterdiameterand, marginally, greaterlength)to occuramongmixedor mammal-dispersed species(signtests,P = .053and P = .115,respectively). resultsin For theothertraitsthatshowedsignificant, or marginally significant, trendis evidentin the theautocorrelation and contrasts analyses,no significant within-genus pairwisecomparisons(table6). To sum up, onlyfruitsize (fruit fruitlength)showcorrelatedevolutionwithtypeof diameterand, marginally, whenphylogenetic are controlled for. seed disperser effects THE AMERICAN NATURALIST 180 0.4 f0.4 A0.2 0.2 0 0 0 0- 0 0 0 00 ui lnt tF Ob 0 F 0 0 00 05 10050 0 0~~~~~~~~0 o 0~~~~~~~~ 0 05 ~0.5 00 . 00. o 0 1 ?2 1. . 0 0 5. 0. )- * -15 *0. ~~ ~~~~~- 0 -0. 0~~~~~ o among----- taxa at the- n 0.5oand trait values 0 .* -1090 00 00~~~ o U) . ~~~~~~- LL 0 dameter s of @6 0 00 - :0:o as of fruitrn Dryimausfragopr son~~~~~~~~Fes 0.5:ral Patte 0 n pce fruit Dri h -- --- -- 0 hlgntccassioficto masso ofri pulp ul on quist (1981).A,~~~ Morhoogia an eintat;B upwtrcnetadntinris Data ointsreprsent compriso amog-dffren-taa-ithn-echhiger-od-ofth Se pupl yieo dmassaina s Dry -0.5threemajorp . of fruitse ereds idsper Numbers sif freiv ofde sotiuees .5Ec masse -0ictre neictre noescotrbuees bdfero eneds aNieauonrsto idsperserrtyp Eachyomthes andtraitvalues amongtaxaat thenode 1 0 1 0. 0orphologicl0 phenotypc variaton can b reduce to hre majrgainsodeg:fut size, including exenldmnin n both~ between al caboydaesan-ipdsad nonstructur0 ibr;ad--"ucuene phentypivaratio as a markednegative-covariation canberdispersero ypreotastsrdinsofdsgn ri tyeagaintithecompari-to ond msedispemrser comparsions bofthe conternastlo FIG, 4.-Plotsg phlgeeier cassifiato ofucroln-e cangiospermasecieand thedsan sowensnonsfuttraituvalue PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 181 0.2 B20.5 0.1 . o.os -0.15 e~~~~~~ 0 ------ % ,A - 0 -- - 0--0** --|---------------- ;^ * ;^ r. | @0 ? 0 --i---- . ! content pergram ~~~~Energy 0.2 02 - a* 0.2 W -0r1 . ; 9 0 'o~~0 - '4 00 10 * 0 p @0 -0.2 0 dPercent water 02ediness) showinde and . o ~ . . * @ content Energy perfruit -0.5 0.0o0.1 bot . i Lipids ~~~~~~*0.2 0.1 0f 0 * 0 00~~~~~~~~~~~. 4~~~~~~~~~~~ 0o 005 0 ,a.-. .j To pulps.~~~~C lag-0et.2rhlgcl n eintais(ie ul loain DiPerser tyecNtrastsutrlcrbhdae grdin, it xtemsdeind o oesie,b hghyfirosfrit,yildn boh are mun f ul ndenry n, n h ohe,fris it atr pulps.To aarge xtent morphlogicl anddesig trait (siz, pul alloation 05 0 T0h o0t strucuracarboydates(asse Proteifcntdifrnoen alus,shoinh02l of C traits (water, majororganiccompo~~~~~Mnentls, fierindmieal) Gauthier- et 005 0l 095 . err 97.1 Asmlreutcoeninflwrg subectito byseedldisprsers nouts moithologyeresultsfrnd,om snelecion, gfrfriet, morphoetricsaeo contraints,e cloustrnt ofnth tontal fruitsihwtr zonesg ofpariulpard 18) ndHner Minerals Fibnd yKche time andphenologicalvaria shouldnoeexxeted;rterth,rneo varia.Tiona ris(ie morphologicaladdsg upallvaration, amongspecieswouldspan mostof thisspace. The oppositetrendwas found, and different familiesand generatendedto clusterat particularcombinations of PC values, showinghighlysignificant differences in thesevariates(also see Gauthier-Hion et al. 1985;Herrera1987).A similarresultconcerning flowering timeand phenologicalvariationwas obtainedby Kochmerand Handel (1986). This outcometherefore variationis largelyan suggeststhatfruitmorphological C) C#4) c C#4)U)) z zz ~~~~~~~~~~~z z - ~~~~~~~~~~~~~~~~~~~~~a 0 4-, C-, C-, ~~~~~~~~~~~~C ~ ~ ~~ ~ ~ ~ ~ ~ ~ ~ OC) OC) ~ ~ ~~C c ) 0 ~~~H ~~~~~~~~~~~~~~~~~~~~~~~~C Z 5 C)~~~~~~~~~~~~~~~~~~~~~~~~~~~<H -~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ - ~ rq C)~ i ~ ~ ~~~~~~~~~~~ -~~~~~~~~~~ ~~~~~~~~~~ ~~~~~~~~~~~~~~~~~~~~~~~~~0 - ~~~~Z ~ ~ ~ ~ ~ ~ ~ ~ -~~~~ -~~~~ ~--4 Z > ; -- PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 183 in this ofhighertaxonomiclevels(family, stableproperty and relatively intrinsic case). offruit"form"and "design"charThe analysisrevealeda markeddecoupling evidentalso whenanaa pattern contentcharacteristics, and nutrient acteristics ofcovariation In fact,theonlypattern matrix on contrasts. lyzingthecorrelation traitswas thatfibrousfruitstendto yielda greater amongdesignand nutrient variation in thesetwomaincomporelativeamountofpulpperfruit.Otherwise, Figure1 shows thatsome families is independent. nentsof fruitmorphology spannedgreatvariationalongPC 1 whileshowinga narrowrangeof scoreson Rutaceae, horizontally, e.g., Melastomataceae, ellipsesoriented PC 2 (confidence Rubiaceae,Ebenaceae, Rhamnaceae).Othersshow the oppositetrend(confie.g., Lauraceae,Smilacaceae,Ericaceae,Paldenceellipsesorientedvertically, (size Meliaceae,Vitaceae).Thefactthatthesetwogradients mae,Flacourtiaceae, infleshy oftotalvariation explainone-half andlipid-soluble carbohydrate content) meansthattheyare twomajorlinesoffamilialdiversification fruit characteristics withinhighertaxa and revealsthatvariationin fruitformand pulpcomposition is boundedby constraints. The precedingresultis notunexpected.Studiesby Sporne(1956, 1976)and reproof angiosperm Stebbins(1951),forexample,indicatethatcharacteristics co-varywithinhighertaxa,sincefloral,carpel,seed, andfruit ductivestructures path(Primack associatedandconnectedalongan ontogenetic traitsareultimately designmostlikelyarisefromdevelopsize andinternal onfruit 1987).Constraints of floralparts,espearrangement imposedby the particular mentallimitations On theotherhand,PCA loadingsforthe of thegynoecium. ciallythestructure expressionof nutrient ofthepulpsuggestthatconservative organicconstituents taxamight be attributable to allocationpatterns among within higher composition of majorcompathways.In addition,certaincombinations majorbiosynthetic pounds (e.g., highwaterand lipid content,or low waterand high solublebe simplyincompatible froma metabolicor physiocontent)might carbohydrate parts of the flowerand fruitare highly logical perspective.That different and showcorrelatedevolutionwas proposedby Vavilov(1922) and integrated by Sporne(1956).These are relevantpointsto a thenestablishedmoreformally rigorousanalysisoffruitand flowerevolutionin relationto seed dispersersand partsof A highlystructured patternof covariationamongdifferent pollinators. theactionofnaturalselectionamongcoevolving does notprevent thephenotype evolutionary change. butitimposeslimitson theresulting partners, PhylogeneticConstraintson Seed Dispersal Syndromes fruitmorphology and seed dispersalagents Previousworkon comparative to the adaptationist hypothesisor, if the potential largelyignoredalternatives (Herrera1986;Desourcesof variationwas acknowledged effectof alternative et al. 1991),no explicit busscheet al. 1987;Willsonet al. 1989;French1991;Lee How is adaptationto was attempted. of its significance important quantification or for fruitvariationnotaccounted by phylogeny seed dispersersin explaining randomeffects? The nestedANOVA analysisshowedthatan averageof 61% of totalpheno- 184 THE AMERICAN NATURALIST in anyangiosperm fruit traitcan be accountedforby taxotypicvariation fleshy nomicaffiliation downto genus.Seed size and seed numberperfruitshowedthe highestphylogenetic variancecomponentvalues,as expectedfromtheirclose relationto flowerand carpellarstructure. Familyeffectswere largeformost traits.These, in contrast,showed designtraitsand smallerforpulp nutrient greatergenericvariancecomponentvalues, whichthusadds evidenceto the ofthisstudy(also see Herrera1987)ofa decoupling ofthetwogroupsof finding traits.Janson(1992)reporteda stronginvariancein thekindsof dispersalsyna resultof dromesevolvedwithinhighertaxa (generaand families),apparently or low adaptivevalue fixeddevelopmental and ontogenetic relatively programs To someextent,phylointermediate oftransitional, forms,betweensyndromes. comestimatetherelativesize of "plesiomorphic" geneticvariancecomponents available for speciesponentsof the phenotype.Littlevariationis therefore specificresponsesto selectionby seed dispersers,since the potentialfor withina givenhighertaxa (e.g., genus)is "nested" withinthis diversification largecomponent ofdescent.Thus,interactions withseed dispersers wereprobaforangiosperm blyrelevantin shapingthemajorlinesofdiversification families and genera,butwe mightexpectverylow evolutionary responseamongcongeMorelocal analyses,witha taxonomicscope nericspeciesto thesemutualists. thantheone used here,can obtaingreaterresolution forthedefinition narrower of dispersertypes,hencemorepowerto testadaptivetrendswithina rigorous framework. phylogenetic of the 16 traitsexaminedheredescribea The phylogenetic autocorrelograms withascendingtaxonomichierarchy. of phenotypic decayingfunction similarity Theyfurther indicatea highlystructured pattern ofvariationrelatedto phylogeofdecreasing with neticaffinity. Thereis a muchsteepergradient autocorrelation levelfordesigntraitsthanforpulpnutrient contenttraits. increasing taxonomic effectsare expectedto be relevantin complexanatomical Since phylogenetic structures or physiological suitesof traits processesthatevolve as integrated (Stebbins1974),thesewill show up moreclearlyin fruitformand structure, attributes offamilies(Cronquist1981).The autoregresconsideredcharacteristic in fruitdesignthanin pulp nutrient sive patternis stronger content,and the formergroupof traitsshowsmorehomogeneouscorrelograms (fig.3), which supportsthisview. werehighly autocorrelation coefficients for11ofthe16 Phylogenetic significant traitsexamined,whichindicatesthata sizablefraction ofphenotypic phenotypic variancecan be accountedforwhenconsidering all phylogenetic simultaneously relatednessamongspecies. Phylogenetic effectsare important for two main groupsof traits,namelyfruitand seed mass and fruitseedinessamongdesign traitsand energycontentperfruit andlipidsamongnutrient contenttraits.Other butlowerR2 values(e.g., fruitdimentraitsshowedsignificant autocorrelations sions,pulpwatercontent, protein).Futurestudiesshouldtherefore payattention to othereffects notexaminedhere(growth form,fruitaccessibility, and color), butsomeanalysessuggesta sizablephylogenetic in them(see, e.g., component Hodgsonand Mackey1986;Willsonand Whelan1990;Chazdon 1991;Fischer and Chapman1993).Whenusingoriginaldata, significant between differences PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 185 betweensynsyndromes were obtainedfornineof the 16 traits.Differences and dromesin fruitlengthand diameter,pulp drymass, energycontent/fruit, forlipidsand pulp mass of determination lipidsremained,and the coefficients relatednesswas accountedfor. halvedwhenphylogenetic were approximately among addressedin thisstudy(i.e., differences Therefore, the firstprediction forphylogenetic effects)is supported syndromes shouldremainaftercontrolling of strict ofthetraitsexamined.However,thefraction onlyin partfora minority small(? 15%). exhibited bythesetraitswas extremely sense"adaptive"variation Dispersal SyndromesRevisited traitsandmajorseed dispersassociationsbetweenfruit Present-day functional ers do notnecessarily implytheircoevolutionas a causal process.All theabove are notinterpretable onlyin indicatethatdispersalsyndromes analysesstrongly a significant histermsofcurrent adaptationto seed dispersersand demonstrate fleshy variationamongangiosperm phenotypic toriccomponentin present-day fruits (also see BremenandEriksson1992;Herrera1992a;Fischerand Chapman varianceaccountedforby highernodes was "subtracted"in 1993).Phenotypic becauseitillustrates theplesiothepreviousanalysesandconsidered nonadaptive are probablya morphicload of thetraits.However,fleshyfruitplesiomorphies and shouldbe incorporated to pastmutualistic interactions resultof adaptations in a comparative analysis. contrastsrevealedtwo strongpatterns.First,a The analysisby independent fruit betweenseed dispersaltypeand mostfleshy correlation lackofevolutionary fruitlengthand pulp lipid traits;in fact,onlyfruitdiameterand, marginally, withtypeof seed disperser.The results contentshoweda trendforcovariation withand supportedthoseof the two previous weretherefore highlyconsistent showeda significant asespeciallydiameter, analyses.Second,fruitdimensions, to increasewithincreasing participation sociationwithtypeofdisperser, tending of crossof mammalsamongthedispersalagents.This supportsearlierfindings et al. 1985; speciesstudiesshowingthesametrend(Janson1983;Gauthier-Hion Dowsett-Lemaire 1988;Debusscheand Isenmann1989; Herrera1989; Willson of significant withthefinding phylogenetic 1993).Thisresultis notincompatible forevolutionary infruit Thepointisthatthepossibilities effects dimensions. change inthesetraitsaretightly boundedbythebauplaninherited byeach species. The evidencefromthe analysisof contrastsand the pairwisecomparisons increasesin fruitsize (diameterand, marginally, demonstrated thatevolutionary associatedwithmixedand mammaldispersal.Studies length)are significantly but on fruitsize are numerous, showinga potentialselectiveeffectoffrugivores to demonstrate conditions fewhave addressedboththenecessaryand sufficient theoperationof naturalselection(Schupp1993;Wheelwright 1993).In contrast selectionon fruitsize has immediate implications to otherfruittraits,frugivore becauseoftheassociationamongfruitsize, on keyaspectsofplantdemography, and successfulseedling seed size, and seedlingvigor;germination probability; selectivepressures I wouldexpectthattheeffects ofpresent-day establishment. causal processes constraints as contributing and phylogenetic or developmental infuturestudieson couldbe dissectedmorefinely coevolution to plant-disperser 186 THE AMERICANNATURALIST particular speciesgroups(e.g., diversified taxa suchas Solanum,or Rubiaceae) in whichcomparative data and well-established can be combined phylogenies withdetailedecologicalexperiments (Bremerand Eriksson1992).In addition, generaltrendssuchas thosedescribedin thepresentstudyforthewholeangiospermclade couldbe testedin smallersubsetsoftheclade (E. Martins,personal Futurestudiesshouldaddresstheshortcomings communication). imposedbythe characteristics of thelargedata base used hereand take advantageof the new ofwell-established comparative methodsand availability combined phylogenies, withrigorousfieldstudiesoffrugivore activity. Allthefruit traitsexaminedshowimportant effects andextremely phylogenetic low potentialforcoevolutionary species-specific adaptationto seed dispersers, probablybecause of constraints and integration imposedby development with structures. A recentmodelfortheevolutionofspecialpredispersal reproductive ized seed dispersalamongvertebrate-dispersed plantspredicteda centralroleof andrapidpunctuated conservatism evolutioninfruit phylogenetic traits(Fleming et al. 1993),and theresultsof thepresentanalysisstrongly supportthisview. But thisis a complicatedsituation.The hypothesis thatfruittraitsevolvedas to seed dispersers butare nowmaintained adaptations otherthan by something selectionis hardtofalsify (Howe 1985),butitis probablycorrectformostindividual fruit traits.The idea ofphylogenetic inertiaand/ordevelopmental constraints implicitly recognizesthattheoriginand maintenance ofadaptationsto seed disdifficult to test(Coddington persersare decoupled,whichmakesthehypothesis 1988;McKitrick1993).The presentanalysissuggeststhatnaturalselectionmight notbe involvedin maintaining adaptationsto seed dispersers, at leastformost fruitphenotypic evolutionwithtypeof seed disperser traits,and thatcorrelated is, at best,onlyevidentforfruitdiameter.To the extentthatthe patternsof covariationbetweenfruittraitsand dispersertypeare epiphenomena of other selectivepressures,suchas flowerdesign,pollinator-derived or physioeffects, on fruitdesign(Cipolliniand Levey 1991; Herrera1992b), logicalconstraints are to be consideredas exaptations(Gouldand Vrba fleshyfruitcharacteristics 1982)to theirpresent-day seed dispersers. The presentstudyand otherrecentanalyses(Bremerand Eriksson1992;Herrera 1992a, 1992b;Janson1992;Fischerand Chapman1993)demonstrate the need to addressthehistoriccomponent of plant-disperser interactions by using bothrigorous methodsandsoundexperimental evidenceforecologicomparative cal effects. theseare keyaspectsforunderstanding Although themechanisms of plant-seeddisperser(also pollinator) coevolutionabove the species level, they wouldbe difficult to integrate. Recentevidenceof multiple typesof constraints on coevolution andOrians1982;Howe 1984;Herrera1986;Jordano (Wheelwright 1987c;Wheelwright 1988;Janson1992;presentstudy)argueagainsta singleforto represent mulation all contributing causalfactorsadequately.Thisis a general issue in evolutionary biologytoday,not specificto the studyof plant-disperser coevolution.A majorproblemis thelack ofa commoncurrency to measurethe effectsof contributing causal processes,and probablytheonlyalternative will be a piecemealapproachto integration (Mitchell1992).Thisexplicitly recognizes theplurality ofcausalprocesses(present-day selection,phylogenetic oneffects, PHYLOGENETIC CONSTRAINTS IN FLESHY FRUITS 187 togenetic constraints, and randomvariation) and thesingularity oftheparticular combination ofeffects and theirsignificance in each particular situation. ACKNOWLEDGMENTS I thankC. M. Herreraand L. Lopez Soria fortheircontinuoussupportand valuablediscussionsand mywifeMyriamforessentialhelpin data preparation; all of themwereextremely patientduringthelonggestationof thisproject.M. withtheanalysesofmostfruitsamplesofCosta Rican Carrionhelpeduntiringly species.Chemicalanalysesof somefruitspecieswereperformed by B. Garcia and A. Garcia,Centrode Edafologiay BiologiaAplicada,Consejo Superiorde Investigaciones Cientificas, Salamanca.Unpublished information was kindlysupplied by F. H. J. Cromeand C. M. Herrera;the latter,L. Lopez-Soria,D. Levey,T. Garland,Jr.,T. Evans,E. Martins, T. H. Fleming, andtwoanonymous reviewers offered usefulcomments to themanuscript; J.M. CheverudandM. F. Willsonmade helpfulsuggestions to earlierdrafts,but theydo notnecessarily H. Luh, and agreewithmyinterpretations. J. M. Cheverud,J. L. Gittleman, A. Purviskindlyprovidedcopies of theirstatistical packagesand programs for comparative analyses.A. Purvisand H. Luh gave excellentadvice and very helpfulassistancewiththeanalysis.My father,D. JordanoBarea, clarified my doubtswithSAS IML programming and alwaysoffered thoughtful suggestions. timeand facilities werekindlyprovidedby theCentrode Informaitica Computer de Andalucia.Financialsupportwas fromtheSpanishDireccionGenCientifica eralde Investigacion Cientifica y Tecnica,projectsPB-87-0452and PB-91-0114, and theConsejeriade Educaciony Ciencia,Juntade Andalucia. LITERATURE CITED ofOfficial methods ofanalysis.Association Chemists.1975.Official Association ofOfficial Analytical Washington, D.C. Analytical Chemists, of leafphenolicsin gap-and and thepatterns Baldwin,I. T., and J. C. Schultz.1988.Phylogeny shrubs.Oecologia(Berlin)75:105-109. forest-adapted PiperandMiconiaunderstory 133:553-571. method.American Naturalist Bell,G. 1989.A comparative characters anddispersalmodesin thetropical Bremer,B., and0. 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