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Seed Dispersal by : Contrasts with Dispersal, Problems of Terminology, and Constraints on Author(s): Nathaniel T. Wheelwright and Gordon H. Orians Source: The American Naturalist, Vol. 119, No. 3 (Mar., 1982), pp. 402-413 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/2460937 . Accessed: 24/12/2013 11:41

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SEED DISPERSAL BY ANIMALS: CONTRASTS WITH POLLEN DISPERSAL, PROBLEMS OF TERMINOLOGY, AND CONSTRAINTS ON COEVOLUTION

NATHANIEL T. WHEELWRIGHT AND GORDON H. ORIANS

Departmentof Zoology, Universityof Washington,Seattle, Washington98195 SubmittedFebruary 27, 1981; Accepted September28, 1981

Recent thinkingabout seed dispersal and the coevolutionof fruitingplants and frugivoreshas been stronglyinfluenced by ideas developed throughthe studyof pollen dispersal by animals. Analogies are commonlydrawn between the two systems (Howe 1977; Van der Pijl 1972; Howe and Primack 1975; Howe and Vande Kerckhove 1979; Howe 1979; Howe and De Steven 1979; Howe 1980). Both systemsrepresent coevolved relationshipsof mutualbenefit to and animalsthat involve the disseminationof pollen or and the provisionby the of some incentivesuch as or .The evolutionof highdegrees of mutual dependence and morphologicaland behavioral specialization,evident in some pollinationsystems, is assumed also to be likelyin certain seed dispersal systems (Howe and Primack 1975; McKey 1975; Howe 1977; Howe and Esta- brook 1977). A rich array of evocative metaphorscurrently used in studies of plant-frugivoreinteractions ("loyalty," "theft," "reliability," "faithfulness," "reward," and so on; see McKey 1975 and Howe and Estabrook 1977) reflects conceptual biases apparentlyderived in part fromimplicit and explicitanalogies withpollen dispersal. Althoughsuch termsare sometimesuseful, they may cloud the true nature of fruit-frugivoreinteractions. Pollen and seed dispersal are fundamentallydissimilar, particularly in most characteristicslikely to influencechoice of diet and foragingitineraries by vectors, and patternsof productionof pollen and fruitby plants. The purpose of this paper is threefold:(1) to outline clearly the relevant differencesbetween pollen and seen dispersal, (2) to indicate some of the problemsof using terminol- ogy borrowedfrom studies of pollen dispersalto describe seed dispersal systems, and (3) to consider the factorsthat may explain the virtualabsence of obligate mutualismsin seed dispersal systems (Howe and Vande Kerckhove 1979). Be- cause of our greater familiaritywith avian frugivoresand their importancein theoreticaland empiricalstudies of seed dispersal, most of our referencesdeal principallywith . Future work on seed dispersalby ,ants, reptiles, and fishmay offernew insights.

Am. Nat. 1982. Vol. 119, pp. 402-413. ? 1982 by The Universityof Chicago. 0003-0147/82/1903-0016$02.00.All rightsreserved. 402

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THE THEORY OF FRUIT- COEVOLUTION Snow (1971) firstconsidered the consequences of evolutionaryinteractions betweenfruiting plants and the frugivoresthat disperse their seeds and recognized theunique attributesof fruit as a food . Relativeto other"prey," fruithas evolved to be generallyaccessible, conspicuous, and easily digestiblein orderto attract seed dispersers (Snow 1971). Following Snow's contribution,McKey (1975) proposed a model of plant-frugivorecoevolution to explain the varietyof strategiesplants use to dispersetheir seeds in whichhe introducedthe concept of dispersalquality. At one extreme,some plantsproduce many small, nutritionally poor fruitsthat attract a wide varietyof "poor quality" dispersers.Alternatively, othersproduce a smallernumber of large,nutritionally superior whose seeds are dispersed by a limitednumber of species delivering"high dispersal quality." Qualityrefers to seed size carriedand the probabilitythat a seed removedfrom a plant is deposited in viable conditionin a site suitable forgermination and estab- lishment(McKey 1975). A numberof recent studies, both theoretical(Morton 1973; Howe and Estabrook 1977; Howe 1979; Thompson and Willson 1979; Fleming 1979) and empirical (Smith 1975; Howe 1977; McDiarmid et al. 1977; Thompson and Willson 1978; Howe and De Steven 1979; Howe and Vande Kerckhove 1979; Howe 1980; Howe 1981; Snow 1981) have refinedhypotheses, evaluated some predictions,and providedobservations on fruitremoval rates and behavior of frugivoresat fruitingtrees. Centralto currenttheory is the propositionthat frugivores differ in behavioral and ecological traitsthat affecttheir suitabilities as seed dispersers.If so, under certaincircumstances (e.g., predictableecological requirementsfor seeds) natural selection is expected to lead to the mutualinterdependence and tightassociation of individual plant species with "one particularlyeffective disperser" (Howe 1977), or a small numberof obligatefruigivores (McKey 1975; Howe and Primack 1975; Howe and Estabrook 1977). However, empirical studies have generally failedto discover eitherhighly coevolved frugivoresor plants adapted to exclude all but a single disperser, as in some (though much fewer than generallyap- preciated) pollen dispersal systems. The lack of plant-frugivorecounterparts to specialized pollinationsystems, such as orchids (Dressler 1968; Dodson 1975) or Dalechampia (Armbrusterand Webster 1979) and euglossine bees, or species and the mothTegeticula (Powell and Mackie 1966), is striking(see also Galil 1977; Sazima and Sazima 1978; Thien 1969). The majorityof studiesof birds, at least, have documentedinstead a tremendousdiversity of frugivoresat fruiting (Eisenmann 1961; Land 1963; Willis 1966; Diamond and Terborgh 1967; Jenkins1969; Leck 1969; Haverschmidt1971; Cruz 1974; Wheelwrightet al., in prep.). Not onlydo manybird species feed on thefruit of a singleplant species, but also they may represent up to 13 families (McDiarmid et al. 1977). Even the "specialized," high reward fruitsof some (McKey 1975) may have theirseeds dispersedby more than 17 species of birdsfrom at least eightfamilies (Wheelwright,in prep.). Morphologicallyas well as taxonomically,birds feeding on the fruitsof the same treemay be quite different(Ricklefs 1977; Wheelwrightet al., in prep.).

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The discoveryof assemblages of manyspecies of diversefrugivores, rather than limitedassociations, spawned a deprecatingterminology to referto species pre- sumed to be poor dispersers: "opportunists,exploiters" (McKey 1975), "fruit thieves" (Howe and Estabrook 1977), and "parasites" (Janzen 1977). Such metaphorsreflect the expectations of the theorymore than they do the actual effectsof the frugivores;data do not yetexist to evaluate accuratelythe effective- ness of dispersalby differentspecies. Despite the factthat many studies purport to deal with seed dispersal, most reportonly observations on who removes fruit, how regularthey are as visitors,and, in some cases, whetheror not theydestroy seeds. The above terminologyobscures the fact thatfrugivores represent a con- tinuumin termsof the numberof seeds each species deposits in suitablesites and the probabilitythat it gives an individualseed favorabletreatment.

SEED DISPERSAL VERSUS POLLEN DISPERSAL Pollen dispersaldiffers from seed dispersalin several fundamentalrespects that preventcomparable precisionin seed dispersal (table 1). First,pollen has a very specific "target," the stigmaof a nonspecificflower. These flowersare usually easily recognizedbecause of theirdistinctive colors, scents, and .In contrast,a seed's "objective," a site suitablefor , establishment, and ultimatelyreproduction, is more difficultto characterizein space and time. Ap- propriatesites for seeds have few distinguishingfeatures perceptible by frugi- vores, althoughfrugivores may preferentiallyfrequent certain types. On a gross scale, some habitat types (flood plains, riverbanks)may be predictable (Howe and Estabrook 1977), but withinthem sites for seeds are not. Moisture, sunlight,soil nutrients,seed and seedlingpredators, , fungal associates, allelopaths,and othersubtle factorsdetermine whether a site is a good one fora seed. Moreover, conditionsmay easily change and characteristicsof a site at the time a seed is deposited may be poor indicatorsof futurequality. Second, pollen dispersaldiffers from seed dispersalin the temporalavailability of suitable sites. Anther and pollen dispersal are coordinated with stigmareceptivity in synchronouslyflowering populations, but opportunitiesfor successful seedlingestablishment (e.g., lightgap formation)may occur randomly in time and space (Poore 1967; Knight 1975; Hartshorn1978). Third,flowering plants benefit from habitat specificity and sequentialvisitation of nonspecificplants by theirpollen vectors because visits to flowersof other species may resultin pollen transferto inappropriate"targets" and consequent waste of pollen. A similaradvantage has been suggestedfor fruiting plants when host-specificfrugivores carry seeds to the habitatsoccupied by nonspecificplants (Howe and Primack1975; Howe and Estabrook 1977). Yet, ifspecies-specific seed and seedling predation is greaternear nonspecifictrees (Janzen 1970; Connell 1971), selection should not favor specialized diets and movementsby dispersers betweentrees of the same species. Moreover,the presence of an adult nonspecific plant is not necessarilyevidence of an appropriatesite fora seed, particularlyin thecase of shade-intolerantplants, which comprise the majorityof species in some tropicalforests (Hartshorn 1978) where up to 90% of plant species are animal dispersed (Frankie et al. 1974). Once a reaches the canopy, its shade

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TABLE 1 GENERALDIFFERENCES BETWEEN POLLEN DISPERSALAND SEED DISPERSAL

PollenDispersal Seed Dispersal

Suitable site for dispersal .... stigmaof conspecificflower site appropriatefor germination and establishment Characteristicsof siteas pre- dictorsof suitability...... distinctive:color, shape, etc.; unpredictable:many subtle oftenapparent at a distance factorsinvolved; present characteristicsoften poor in- Temporalpattern of suitable dicatorsof futurequality sites ...... synchronouswith pollen dis- unpredictable:often inde- persal pendentof habitattype or phenologyof nonspecific Advantagefor plant of diet and plants habitatspecificity by animal vector ...... high:most pollen lost if visitsto low: presence of adult con- other species of plants inter- specificplant often an unsuit- vene between visits to con- able site because of density- specifics dependent seed predationor Abilityof plant to directanimal differenthabitat requirements vectors to suitable site .... of seed and tree high: incentives(nectar, pollen, low: no incentivefor frugivore etc.) provided at suitable site to deposit seed in favorable site; seed representsheavy and space-consumingballast thatis profitablydiscarded as quickly as possible.

has changed the favorable microhabitatthat allowed its own establishmentas a seed and seedling. Perhaps the most fundamentaldistinction between pollen dispersal and seed dispersal systems is the abilityof the plant to manipulatethe behavior of the animal vector. Floweringplants can controlpollinators' movements to a greater extentby providingnutritional (Baker and Baker 1975) and reproductive(Dodson 1975) incentivesat the appropriatesite ()for pollen transfer.There is, in effect,"payment upon delivery." There is no similarincentive for seed dispersers to drop seeds in appropriateplaces. Fruitingplants sufferthe costs of "advance payment": Once frugivoreshave strippedseeds of theirnutritious fruit, there is no furtheradvantage in carryingthe "ballast" (Snow 1971) which, unlike pollen, may be heavy and space consuming.Hence, rapid regurgitationor defecationof the seed benefitsthe disperser,irrespective of its advantageto the plant. For both pollinatorsand frugivores,the delayed returnbenefits of "altruistic" pollen or seed dispersal(such as futureincreases in local floweror fruitavailability) may be discounted (see also Howe and Estabrook 1977). Given these limitations,to what degree mightplants be able to manipulatetheir potentialseed dispersers?It has been suggestedthat morphological, chemical, and phonologicalcharacteristics of plants and theirfruits may induce frugivoresto leave fruitingtrees afterconsuming few fruits.Among the conceivable incentives are limited levels of fruitproduction (Howe 1977), mild toxicity, nutritional

This content downloaded from 139.140.232.150 on Tue, 24 Dec 2013 11:41:24 AM All use subject to JSTOR Terms and Conditions 406 THE AMERICAN NATURALIST inadequacy of fruits,bulky or slowlydigestible fruits, and structuralmodifications of the plantto increase the riskof predation.Whether these are "adaptations" or consequences of otherlife history demands (defense against fungal,bacterial, or fruitand seed parasites; limitationsof energyor nutrients;photosynthetic considerations,etc.) remainsuncertain at this point. In any event, plants cannot directthe dispersal of seeds to a particularlocation with a degree of exactness comparable to pollen dispersal, thoughpossibly theycould favoranimal vectors withparticular behaviors (Docters van Leeuwen in McKey 1975), habitatprefer- ences, or probabilisticpatterns of seed dispersal (Smith 1975; Howe 1977; Howe and Primack 1975). Thus, environmentalunpredictability and the difficultyof directingseed vec- tors, even if suitable sites were "knowable," constrainseed dispersal systems fromachieving the precisionand specializationof some pollen dispersal systems.

"SPECIALIZATION" IN PLANT-FRUGIVORE INTERACTIONS Justas comparisonswith pollen dispersal have led to unrealisticexpectations about coevolved mutualismsin seed dispersalsystems, imprecise and inconsistent terminologyhas affectedtheoretical developments and interpretationof empirical observations.For example, the term"specialist" is used frequentlywith respect to fruit-frugivoreinteractions. Basically theterm refers to theuse of onlya portion of the totalarray of available resources. No organismis a pure generalist,using all potentialresources in proportionto theiravailability, but, because species differ in the extentto which they are selective in resource use, the term "specialist," even thoughit is inevitablyimprecise, is useful for comparingspecies. A firstsource of confusionarose because the degreeto whicha frugivoreshould be considereda "specialist" has been assessed by differentcriteria: being totally or mostly frugivorous(Snow 1971); feeding only fruitto its nestlings("total frugivory";Morton 1973); relyingsolely on fruitas its source of proteinand lipids (McKey 1975); and beingan animalthat is "totallydependent on fruitfor food for at least part of its life and which invariablyvoids or regurgitatesseeds in viable condition" (Howe and Estabrook 1977,p. 818). Snow (1981) definesa specialistin termsof the qualityand size of the fruitsit eats. The bearded bellbird(Procnias averano) is oftencited as the archetypal"specialist" (McKey 1975), despite the fact that it actually feeds on at least 40-50 species of fruit(Snow 1970) and probably and lizards as well (based on personal observationsof its con- genor P. tricarunculataand other tropical frugivores).All of the above notions have value, but the use of a singleterm to referto such disparatecharacteristics is certainto fostercontinued confusion. It would be preferableto use more precise termsto referto particularpatterns of resource use, such as "principallyfrugivo- rous." Moreover, the term "specialist" is totallyinappropriate when applied to characteristicsunrelated to resource use, such as dispersal quality. A second problem arises with respect to the concept of a "specialized dis- persal system." Specialization in plant-animalmutualisms has two components that must be distinguished.A fruitingplant, for example, may specialize with regardto its seed dispersers:Its seeds may be principallydispersed by onlyone or

This content downloaded from 139.140.232.150 on Tue, 24 Dec 2013 11:41:24 AM All use subject to JSTOR Terms and Conditions COEVOLUTION OF FRUITING PLANTS AND FRUGIVORES 407 a few of the arrayof potentialfrugivores. A fruit-eatinganimal, in turn,may be a specialist by restrictingthe major part of its diet to a small subset of the fruits available. In principle,therefore, a plant could specialize on a few generalist dispersers,just as a frugivorecould specialize on a plant dispersed by many species. Moreover, there is no a prior reason to expect a strong correlation between the degree of specialization and the importanceof a plant to a frugivore and vice versa. A frugivoremay be veryimportant to a plantin a situationwhere neitherthe plantnor the frugivore is a specialist(e.g., thetree Casearia corymbosa [=C. nitida] and the masked tityra,Tityra semifasciata; Howe and Primack1975; Howe 1977; also Noble 1975). Pollen and seed dispersal systemsdiffer in the extentto which plants benefit fromspecialization, either in terms of being dispersed by a limitednumber of potential dispersers or attractingdiet-specific animal vectors. In the case of floweringplants, entrainedpollinators reduce the incidence of hybridizationand wasted investmentin lost pollen and inviable seeds, and increase the amount of pollen deliveredto suitablesites. Pollinationby species-specificvectors allows the persistenceand reproductionof plants when populationdensities are low (Baker and Hurd 1968; Janzen 1971). Because of the relativeprecision of pollen transfer, natural selection can favor the evolution of complex flowersthat exclude or discourage organismsunlikely to transferpollen to nonspecificstigmas with little adverse effecton pollinationsuccess. Not surprisingly,there are examples of flowersthat attractonly one or a few pollinatorswith narrowdiets ("specialize on specialists"; see referencesabove). The potentialvalues to plants of having only a few kinds of seed dispersers depend on both treatmentof seeds and the way they are deposited into the environment.If only a singlefrugivore species regularlyvisits a plant,most of the plant's seeds receive similartreatment. Either seeds will be regurgitatedor, ifthey pass throughthe digestivetract, they will encountersimilar chemical and physical conditions(McKey 1975). Therefore,an optimalseed coat just sufficientto with- standthe abrasion receivedby the seed in thegut of the frugivore,but not so tough as to inhibitsubsequent germination or cause waste of resources in the construc- tion of unnecessarilystrong coats, can evolve. Birds thatrely on fruitsfor all or nearly all of their nutritionalneeds are believed to have soft-linedgizzards (McKey 1975), and many of them regurgitateseeds. However, it is likely that soft-linedgizzards evolved to avoid digestionof toxic, thin-coatedseeds rather than to provide gentletreatment to the seeds, and regurgitationis advantageous because it quickly reduces the indigestibleballast carried by the frugivore. In general, the smaller the numberof species of frugivoresthat visit a plant species, the fewerthe habitattypes in which its seeds are likelyto be deposited. However, withinthose ,suitable sites for seed germinationand seedling establishmentmay arise unpredictably.Because of seed dormancyor seedling longevity,sites may be occupied long beforethey arise (Howe 1980). Therefore, unless there are strong temporal correlations between the sites visited by a particulardisperser and the present or futureavailability of suitable sites, the potentialadvantage of havingonly a restrictedset of seed dispersersmay not be realized (Howe 1977).

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Set against these possible advantages of restrictingthe array of frugivores regularlyvisiting a plant,there are a numberof advantageslikely to be associated withattracting many kinds of dispersers.First, the largerthe numberof species of frugivores,the greaterthe number of dispersingindividuals and the larger the numberof fruitsthat can be removed fromthe tree per day (Snow 1971). Since fruitsmay oftenrot on trees or fall to the groundwithout having been consumed (personal observation; Howe 1981), there are often situationsin nature when having more visitorswould probably be beneficial. Second, a fruitcapable of being dispersed by a varietyof frugivoresis not limitedto the habitat or general geographical range of any single disperser (a restrictionin some pollinationsystems; Baker and Hurd 1968) and can expand its distributionto colonize new sites (Hamilton and May 1977). Third,plants that rely on manyspecies to dispersetheir seeds may have a lower probabilityof extinctionif a single disperserbecomes extinctor becomes very rare (Howe 1977; Howe and Vande Kerckhove 1979; 1977; Gilbert1980). However, the evolutionof such "bet-hedging"strategies has yet to be supported by genetic models of natural selection at the level of the individual(Slatkin and MaynardSmith 1979). High rates of populationturnover, probably even greaterin the tropicswhere many species have low populationdensities and poor dispersal abilities(Willis 1974), may mean thatfruiting plants are rarelyin association long enough with specificfrugivores to evolve tightobligate mutualismseven if they were favored over the shortterm. Fourth, even thoughthe mean probabilityof seed survival mightbe lower in seed distributionsproduced by dispersersof many species than in distributions produced by a singlehigh quality disperser,natural selection could favorattract- ingmany dispersers rather than a singleone (fig.1). Whetheror not the right-hand tail of the seed distributioncurve generatedby manydispersers lies furtherto the rightthan thatgenerated by a singledisperser depends, of course, on the relative availabilitiesof dispersersand on theirbehavior. But since a tree may produce hundreds to millions of seeds duringits lifetime,each with an extremelylow probabilityof survival (given the fact that each plant , on average, one offspringin an equilibrialforest), counting on a singledisperser may be analogous to Williams' (1975) assessment of asexual :the multiplepurchase of the same lotteryticket. Unfortunately,testing this hypothesisdirectly is extremelydifficult. Of the many seeds produced, findingthe survivingseedlings is difficult.Knowing their parents and their dispersers seems almost hopeless. Althoughthe probability of survival of any one seed is extremelylow, whetheror not the possibilityof improvingthat probability is favoredby naturalselection depends on the value of alternativeuses of energyby the plant. For adult plants that have reached the canopy or theirnormal full size, alternativeuses of energyor nutrientsshould normallyhave verylow marginalvalues, favoringheavy investmentsin reproduc- tion even when the marginalvalue of incrementsto reproductiveinvestments are as low as theynormally must be formost plants. The real meaningof "waste" in seed dispersal (Howe 1980) is thereforeunclear. Viewing the problem fromthe point of view of frugivoresalso suggests that under most circumstanceseating a varietyof fruits,plus animal foods as well,

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Dispersal by many species In addition ( to 'sigh quality disperser w (I)

0~

(n | \ispersa/ by "high quality" 0 w >(! /disperser a/one w

LAL 0/ W~~~~~~~~~~~~~~~~~~~~

D/

zTALLLOW /PECIE5) X// GH OUAL/TY A DL(PERLER S HI GH SUITABILITY OF SITES IN WHICH SEEDS ARE DEPOSITED

FIG. 1. Suitabilityof seed dispersal by a wide assemblage of dispersers(solid line), versus by a single "high quality" disperser(dashed line). If only those seeds deposited in the best sites (to the rightof pointA) are likelyto survive,natural selection will favorthe attractionof a diversedisperser assemblage in spiteof itslower mean dispersalquality (cf. Williams1975).

should normallybe favored. Very few plants fruitthroughout the year, and few are commonin morethan a limitedpart of theirrange. Moreover, mostfrugivores (with the exception of ants) are moderate-sized,relatively long-lived organisms thatcannot package theirannual cycle withina singlefruiting season the way that manypollinators do. Not surprisingly,a numberof large, principallyfrugivorous birds undergo marked seasonal movementsduring the year in response to local variations in fruitabundance (personal observation). Few dispersers are con- stantlyreliable in the sense of McKey (1975) and Howe and Estabrook (1977). Also, frugivoresthat may provide highquality dispersal at one timeof the year may not do so at other times. The obligately frugivorousoilbird (Steatornis caripensis) roosts and nests in caves where most of the seeds it ingests are deposited (Snow 1962); bellbirds and manakins typicallydrop seeds beneath displayperches duringthe breedingseason (personal observation).Although they probablygive all seeds gentletreatment, they are usually low qualitydispersers at such times in termsof the sites where they deposit seeds.

CONSTRAINTS ON COEVOLUTION We have argued that finelytuned mutualisticrelationships in seed dispersal systemsshould be rare forthe followingreasons: (1) the inabilityof the plant to provide incentives for precision in seed dispersal; (2) the relativelysmall dif-

This content downloaded from 139.140.232.150 on Tue, 24 Dec 2013 11:41:24 AM All use subject to JSTOR Terms and Conditions 410 THE AMERICAN NATURALIST ferencesamong frugivoresin seed dispersal quality; (3) the unpredictabilityand difficultyof recognitionof suitable targetsfor seeds; (4) the potentialadvantages of having a broad assemblage of dispersers; and (5) the nature of life cycles of frugivores.There may also be evolutionaryconstraints on developinga restricted assemblage of seed dispersers (cf. Janzen 1977). For example, in Costa Rica's lower montane wet forest,both mountainrobins (Turdus plebejus) and - throatedrobins (T. assimilis), as well as many otherspecies, feed on lauraceous fruits.The habitat preferencesand foragingpatterns of the two species differ markedly(personal observation). They may also differin some measure of dis- persal quality, yet it is difficultto imaginewhat adaptationsa plant could use to exclude the poorerdisperser without barring its morphologicallysimilar congener as well. Classes of disperserscould be favoredby alteringfruit size (McKey 1975; Howe and Estabrook 1977), heightof presentation(L. Best, in prep.), firmnessof attachment,color, nutritionand manyother features. These traits,however, are likely simplyto reduce the diversityof visitors(possibly excluding some good dispersers), not to limitit to a single species. Equally importantmay be the influenceof spatial heterogeneityand flow (Howe and Vande Kerckhove 1979). Geographicalregions differ in the proportion of habitattypes and the pool of available dispersers. Even over relativelyshort distances totally differentfrugivores may feed on the fruitsof the same tree species. Thus, if thereis gene flowbetween populationsof a tree species, it may not evolve adaptationsto exclude poor dispersersin one area because the same tree in anotherplace is visitedby a differentgroup of brids. Gene flowprobably constrainscoevolution of one-to-onemutualisms in pollinationsystems as well. Under what conditions would one expect to find highlycoevolved mutual- isms between fruitingplants and frugivores?Two accounts document obligate mutualisms(from the plant's perspective;Rick and Bowman 1961; Temple 1977). Interestingly,both of these associations occur on islands,where environments are relativelyuniform, faunas are impoverished,and populationsare isolated fromthe homogenizinginfluence of .

SUMMARY Theoretical and empiricalresearch on frugivoryand seed dispersal has been influencedby concepts derived from the study of . In particular, explicit and implicitanalogies between seed dispersal and pollen dispersal have led to the expectation, under certain conditions, of the evolution of obligate, species-specificrelationships between fruiting plants and the animalsthat disperse theirseeds. The two systemsdiffer in importantrespects, however. Plantsbenefit by directingpollen dispersersto a definite,recognizable "target," a nonspecific flower,and theycan provide incentivesat flowerswhich serve to attractpotential .In effect,there is "paymentupon delivery" of the pollen. In contrast, for seeds the target(an appropriate site for germinationand establishment)is seldom readilydiscernible, and dispersalbeneath a nonspecificplant may actually be undesirable. Another importantdifference is that frugivoresare "paid in advance." Because of these differencesand others,the outcomes of coevolution

This content downloaded from 139.140.232.150 on Tue, 24 Dec 2013 11:41:24 AM All use subject to JSTOR Terms and Conditions COEVOLUTION OF FRUITING PLANTS AND FRUGIVORES 411 of fruitingplants and frugivoresare expected to be differentthan those of flower- ing plants and flower visitors. There are thereforeproblems with drawing analogies between the two systemsand usingterminology derived from studies of pollinationto design and interpretstudies of seed dispersal.

ACKNOWLEDGMENTS We appreciate the interestand insightscontributed by the and Evolu- tionaryBiology groupat the Universityof Washingtonduring various discussions of these ideas. L. Best, M. Gardner,W. Haber, H. Howe, S. Koptur, E. Leigh, and A. Worthingtonoffered helpful comments on an earlierdraft. A suggestionby M. Westoby prompted the use of fig. 1. The firstauthor received generous financialsupport fromthe Organizationfor Tropical Studies and Sigma Xi for research in Costa Rica.

LITERATURE CITED

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