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Seed Dispersal by Animals: Contrasts with Pollen Dispersal, Problems of Terminology, and Constraints on Coevolution Author(S): Nathaniel T

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Seed Dispersal by Animals: Contrasts with Pollen Dispersal, Problems of Terminology, and Constraints on Coevolution Author(S): Nathaniel T The University of Chicago Seed Dispersal by Animals: Contrasts with Pollen Dispersal, Problems of Terminology, and Constraints on Coevolution 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 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 [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org 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 Vol. 119, No. 3 The AmericanNaturalist March 1982 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 plants and animalsthat involve the disseminationof pollen or seeds and the provisionby the plant of some incentivesuch as nectar or fruit.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 animal 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 birds. Future work on seed dispersalby mammals,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 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 403 THE THEORY OF FRUIT-FRUGIVORE COEVOLUTION Snow (1971) firstconsidered the consequences of evolutionaryinteractions betweenfruiting plants and the frugivoresthat disperse their seeds and recognized theunique attributesof fruit as a food resource. 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 fruits 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 yucca 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 trees (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 Lauraceae (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.). 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 404 THE AMERICAN NATURALIST 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 morphology.In contrast,a seed's "objective," a site suitablefor germination, 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 habitat 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, herbivores, 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
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