Effects of Resource Distribution on Animal–Plant Interactions || How Do Fruit- and Nectar-Feeding...

12 How Do Fruit- and Nectar-

Feeding Birds and Mammals Track Their Food Resources?

Theodore H. Fleming Department of Biology

University of Miami Coral Gables, Florida

I. I n t r o d u c t i o n I I . Resou rce Variabil i ty in T h e o r y a n d Pract ice

A. Resource Variabil i ty in T h e o r y B . R e s o u r c e Variabil i ty in Pract ice

I I I . Responses by F rug ivores a n d Nec ta r ivores to Resou rce Variabil i ty A. D e m o g r a p h i c Responses B . M o v e m e n t s C. Social Responses

IV. Conc lus ions A p p e n d i x Refe rences

I. Introduction

C o m p a r e d with o t h e r diet classes, frugivory a n d nectar ivory a r e r a t h e r u n c o m m o n feeding specializations in b i rds a n d mammals . In a recent review of the evolut ionary history of fruits a n d frugivores, I identified only 12 avian families, conta in ing about 600 species, a n d eight m a m m a l i a n families, conta in ing abou t 460 species, as be ing principally frugivorous in diet (Fleming, 1991). Similarly, only th ree major families of birds (Trochi l idae , Nec-tar ini idae, a n d Melaphag idae ; about 630 species), plus p e r h a p s 200 addi tional species in several o the r families (Collins a n d Paton, 1989), a n d only two families of bats (P te ropod idae a n d Phyllostomidae; less t han half of

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356 Theodore H. Fleming

the i r 310 species a re strongly nectar ivorous) , a handfu l of pr imates , a n d the marsupia l Tarsipes rostratus regular ly include nectar a n d pollen in their diets. T o g e t h e r , these two diet g roups r ep re sen t about 17% of the c u r r e n t diversity of b i rds a n d mammals . Despite this relatively low taxonomic diversity, avian a n d m a m m a l i a n fruit- a n d nectar-eaters play ext remely impor t an t roles as seed d ispersers a n d pol l inators in terrestr ial ecosystems, especially in the tropics (Bawa, 1990; Fleming, 1988; Stiles, 1985).

Like all animals , frugivores a n d nectar ivores spend most of their lives finding a n d eat ing food. T h e p rob lems that frugivores a n d nectar ivores face in feeding, however , a re not necessarily the same as those faced by herbivores a n d carnivores ( including insectivores), the o the r major diet classes of m a m m a l s a n d birds . Plants often de fend their tissues morpho log i cally, chemically, a n d phenologically against consumpt ion a n d assimilation by herbivores (Chapte rs 7 a n d 10). Similarly, an imal prey species use a wide variety of m e t h o d s to r e d u c e their detect ion a n d consumpt ion by carnivores (Chap te r 8). As a resul t of p lant defenses, herbivores probably spend m o r e t ime processing t han locating food, whereas the opposi te is usually t rue of carnivores .

In contras t to herbivores a n d carnivores , which generally have an tagonistic re la t ionships with the i r food species, frugivores a n d nectar ivores general ly have positive, mutualist ic relat ionships with their food species. Plants offer a nut r i t ional r eward to animals in the form of seed-filled fruits a n d nectar- a n d pol len-conta in ing flowers in exchange for increased mobility for the i r seeds a n d pol len grains . T h o u g h basically positive, these p l a n t -animal interact ions a re uneasy partnerships (Howe a n d Westley, 1988) that involve conflicts of interest be tween plants a n d their d ispersers a n d pollina tors . Th i s conflict results f rom plants r equ i r ing m o r e mobility for thei r seeds a n d pol len t han animals , which a r e selected to maximize net ene rgy gain p e r uni t of foraging t ime, a re willing to give. Resolution of these conflicts probably se ldom occurs for a variety of reasons , including the effects of climatic seasonality on dietary general izat ion, interspecific differences in foraging behavior , a n d the lack of cong ruence in p lan t a n d animal dis t r ibut ions (Howe, 1984; H e r r e r a , 1986). Plants can, however , man ipu la te frugivore and , to an even g rea te r extent , nectar ivore foraging behavior with a variety of morphologica l , nutr i t ional , a n d phenological me thods (Feinsinger, 1983, 1987; Wheelwr igh t a n d Or ians , 1982).

A l though fruits a n d flowers a re often conspicuous a n d easily located, these foods a re general ly descr ibed as be ing patchy a n d ephemeral C o m p a r e d with o the r kinds of foods, especially insects, fruit a n d flower densities a re usually cons idered to be qui te variable in space a n d t ime. Assuming for the m o m e n t that this is t rue , my goal in this chap te r is to exp lore the ways in which this resource variability influences the ecology a n d behavior of avian a n d m a m m a l i a n frugivores a n d nectar ivores. I will pay par t icular a t tent ion to the effect resource variability has on the d e m o g r a p h y a n d a b u n d a n c e ,

12. Resource Tracking in Frugivores and Nectarivores 357

daily a n d seasonal movemen t s , social organizat ion, a n d ma t ing behavior of these b i rds a n d m a m m a l s . O n e of the major points that will e m e r g e f rom this chap t e r is tha t the lives of many species of fruit- a n d nectar -ea ters ope ra t e on a la rge spatial scale. E p h e m e r a l , patchy resources select for h igh mobility, which, as we will see, can p ro found ly affect m a n y aspects of the lives of frugivores a n d nectar ivores . An excellent overview of an imal r e p o n -ses to patchy env i ronmen t s can be found in Wiens (1976).

I I . Resource Variability in Theory and Practice

A. Resource Variability in Theory T o maximize lifetime fitness, animals should closely track resources . Th i s t racking can involve at least four different aspects of their life histories:

1. demography /phys io logy , inc luding the t iming of b reed ing , molt , a n d to rpo r , o r h ibe rna t ion ;

2. daily a n d seasonal foraging movemen t s ; 3. social organiza t ion , inc luding in t ra a n d interspecific social interact ions,

such as terr i tor ia l a n d / o r g regar ious behavior ; a n d 4. m a t i n g systems, i.e., m o n o g a m y versus polygamy.

Points 3 a n d 4 have been discussed in C h a p t e r 3, bu t on a m u c h finer spatial scale t h a n cons ide red he r e . T h e major work ing hypothesis in this c h a p t e r is tha t these four life-history c o m p o n e n t s of frugivores a n d nectar ivores a re affected, at least in par t , by pa t t e rns of resource variat ion. A second hypothesis is tha t the life histories of frugivores a n d nectar ivores differ significantly f rom those of insectivores, the diet class f rom which frugivory a n d nectari-vory have evolved.

Resource variat ion a n d resource t racking have bo th spatial a n d t empora l aspects. A l t h o u g h space a n d t ime a re con t inuous variables, I find it convenient to recognize at least two d imens ions for each of these variables. Space has t h r e e i m p o r t a n t d imens ions—la t i tude , longi tude , a n d e levat ion—in the lives of m a n y frugivores a n d nectar ivores . As discussed in detail later, the a n n u a l cycles of m a n y species involve significant spatial shifts a long each of these d imens ions . Similarly, the t ime variable can be subdivided into several d imens ions , inc lud ing daily, weekly, a n d month ly , o r longer , t ime blocks. In genera l , because nec ta r availability can change substantially on an hour ly basis (e.g., H ixon et aL, 1983; McFar land , 1986; Pyke, 1988), t empora l variat ion probably occurs on a finer scale for nectar ivores t han it does for frugivores. Frugivores a n d nectar ivores thus live in mul t id imens ional worlds bo th spatially a n d temporal ly , a n d we expect the i r life histories to reflect the variability unde r ly ing this dimensional i ty.

W h a t a re the expec ted re la t ionships be tween resource variability a n d the life histories of f rugivorous a n d nectar ivorous b i rds a n d mammals? T o


begin to answer this quest ion, consider the two env i ronment s depicted in Figure 1. E n v i r o n m e n t A completely lacks s p a t i o - t e m p o r a l variation in the n u m b e r of food species (40) available each m o n t h over a wide r ange of lat i tudes. In contrast , the n u m b e r of food species available in E n v i r o n m e n t B varies widely in t ime a n d space. S p a t i o - t e m p o r a l resource variability (patchiness) is absent in E n v i r o n m e n t A a n d is h igh in B. Resource t racking prob lems clearly a re m o r e acute in Env i ronmen t B than in A. C o m p a r e d with an o rgan ism living in E n v i r o n m e n t A, an organism in Env i ronmen t B should have a m u c h m o r e strongly seasonal a n d less-sedentary life history at all lat i tudes. In E n v i r o n m e n t B, b r e e d i n g should be m o r e strongly seasonal; socially media ted spacing pa t te rns a re likely to vary seasonally; social systems are m o r e likely to be gregar ious than intolerant ; a n d individuals a re m o r e likely to migra te or switch to a n o t h e r food type (Wiens, 1976). As discussed below, the worlds of real-life frugivores a n d nectarivores a re m o r e like E n v i r o n m e n t B than A.

T h e two env i ronmen t s in F igure 1 provide a visual p ic ture of s p a t i o -t empora l patchiness, bu t it would be useful to have a m o r e quanti ta t ive definition of the t e rm patchy. Intuitively, such a definition might be obta ined by calculating resource state changes in an m by n mat r ix consisting of m t empora l co lumns a n d n spatial rows. Patchy env i ronmen t s will have h igher rates of change a n d m o r e ex t r eme values from one cell to a n o t h e r t han will non-pa tchy env i ronmen t s . Evaluat ing the m a g n i t u d e of resource levels in each cell of the mat r ix in relat ion to an animal 's energet ic needs for reproduc t ive , social, a n d migra tory purposes would allow us to answer such quest ions as: W h e n a n d whe re should a species breed , de fend resources , form pair bonds o r ma te polygamously, jo in foraging g roups , o r migrate?

S p a t i o - t e m p o r a l resource variability mus t be viewed in relat ion to the body size a n d locomotory adapta t ions of frugivores a n d nectar ivores. Sizes of avian frugivores r a n g e f rom abou t 0.010 kg (small tanagers) to 2 to 3 kg (hornbills), a n d f rom 0.005 to 1 kg in bats. Sizes of a rborea l o r terrestr ial avian frugivores r ange f rom 0.25 ( t inamous) to 58 kg (cassowaries), a n d in a rborea l mammals , f rom 0.40 ( tamarins) to 150 kg (orangutans) . Ter res t r ia l mammal i an frugivores r ange f rom 0.020 (rodents) to 7,500 kg (African e lephant ) . Nectar ivores a re generally smaller than frugivores. Sizes of avian nectar ivores r a n g e from 0.002 (hummingbi rds ) to 0.15 kg (wattlebirds) a n d from 0.008 to 1 kg in bats. Nectar ivorous arboreal mammals r ange from 0.013 (Tarsipes) to abou t 3 kg (in Cebus monkeys , which a re only partially nectar ivorous) .

Size is impor t an t because we expect the effects of resource and climatic seasonality to decrease as body size increases in both birds a n d mammals ; small species generally live in m o r e coarse-grained env i ronments than d o large species [see discussions in Calder (1984) and Peters (1983)] . Likewise, aerial species can m o r e easily track spatially variable resources and can evade seasonally lean or physiologically ha r sh times of the year by migra t ing


Figure 1 R e s o u r c e var ia t ion, m e a s u r e d as t he n u m b e r of food species available p e r m o n t h , in two ideal ized e n v i r o n m e n t s . Values in I B w e r e g e n e r a t e d by select ing pa i rs of r a n d o m n u m b e r s for each m o n t h at la t i tudes 0, 10, 20, 30 , a n d 40.


t han can terrestr ia l o r a rborea l species. Because of their g rea te r mobility, we expect a g rea te r n u m b e r of aerial b i rds and mammals to be commi t ted frugivores a n d nectar ivores yea r - round than a re a rborea l o r terrestr ial species.

B. Resource Variability in Practice H o w variable in t ime a n d space a re real-world fruit a n d nectar resource levels? T o m o r e fully u n d e r s t a n d the evolution of ma t ing systems in New Guinea b i rds of paradise , Beehler (1983) indicated that m o r e informat ion was n e e d e d on spatial d ispers ion of different food plants , size of fruit crops , intraspecific synchrony in fruit r ipen ing , length of fruit ing seasons, annua l predictabili ty of frui t ing cycles, a n d the nutr i t ional composi t ion of fruit. Ob ta in ing all of the informat ion in this "wish list," a n d d e t e r m i n i n g annua l variat ion in fruit/flower c rop sizes, would seem to be essential for u n d e r s tand ing the behavioral ecology of frugivores and , by subst i tut ing flowers for fruits in the list, of nectar ivores. Not surprisingly, however , such complete resource informat ion is rarely available for any study system [for an except ion, see H e r r e r a (1984)] , so we current ly have an incomple te p ic ture of the resource env i ronmen t s of most species of frugivores a n d nectarivores.

C u r r e n t informat ion abou t fruit a n d flower resource env i ronmen t s generally suppor t s the hypothesis that these resources a re indeed patchy in t ime a n d space. For example , in the handfu l of studies that have m e a s u r e d t empora l a n d / o r spatial variat ion in animal a n d plant resources in the same study area , fruit a n d flower a b u n d a n c e appea r s to be m o r e variable than insect a b u n d a n c e (Karr , 1976; Mar t in a n d Karr , 1986a; Pyke, 1983).

Ra the r t han exhaustively review fruit a n d flower resource pa t te rns , I shall i l lustrate genera l phenological t r ends with selected sets of data . More extensive reviews of these topics can be found in Baker et al (1983), Feinsinger (1987), F l e m i n g ^ / . (1987), Pr imack (1987), a n d R a t h c k e a n d Lacey (1985). T w o b r o a d lat i tudinal pa t t e rns exist r e g a r d i n g seasonal t r ends in the n u m ber of fruit ing a n d flowering plants :

1. seasonality increases with increasing lat i tude, a n d 2. species diversity decreases with increasing lat i tude (Fig. 2).

At midla t i tudes in the t e m p e r a t e zone, the availability of fleshy fruits is highest in the a u t u m n a n d winter , a n d lowest in the spr ing a n d s u m m e r ; it is highest d u r i n g rainy seasons a n d lowest at wet-to-dry-season transit ions in most tropical habitats . Flowering peaks occur in the s u m m e r in the eas tern Uni ted States, bu t in the winter a n d spr ing in sou theas te rn Austral ia (Paton, 1985a). T h e d ry season (December t h r o u g h March) contains peak flower n u m b e r s for nec tar ivorous bats in Cent ra l Amer ica (Hei thaus et al, 1975), bu t h u m m i n g b i r d flower peaks occur in bo th the dry a n d wet seasons (Fig. 2).

Figs a re p e r h a p s the archetypical patchy fruits. C o n s u m e d by a wide


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Month Figure 2 M o n t h l y c h a n g e s in t h e n u m b e r of f ru i t ing o r flowering species p r o v i d i n g food

for b i rd s at t h r e e la t i tudes in t h e N e w W o r l d . F r o m Aus t in (1975), F r a n k i e et al. (1974) , Skea te (1987) , Stiles (1980) , T h o m p s o n a n d Willson (1979) .

3 6 2 Theodore H. Fleming


Figure 3 Mon th ly c h a n g e s in t he n u m b e r of f ru i t ing o r flowering species p r o v i d i n g food for b i rds in t h r e e habi ta ts at La Selva, Costa Rica (3A a n d 3B , respectively) a n d at fou r e levat ions (100, 1000, 1300, a n d 3000 m) in Costa Rica (3C). Habi ta t s in 3A: 1, edges a n d second g r o w t h ; 2, forest u n d e r s t o r y ; 3 , forest canopy . Habi ta t s in 3 B : 1, s econd g r o w t h ; 2, gaps in p r i m a r y forest ; 3 , p r i m a r y forest u n d e r s t o r y . F r o m Fe ins inger (1976), Levey (1988), Stiles (1980, 1985b), Wolf et al. (1976).

variety of oppor tun is t ic a n d specialized tropical frugivores ( T e r b o r g h , 1986), most species of Ficus p r o d u c e e n o r m o u s bu t short-l ived crops of nutr i t ionally p o o r fruit. Owing to intraspecific asynchrony in syconia ( the technical n a m e for the fruit/flower unit) p roduc t ion a n d low popula t ion densit ies, fig crops can be widely separa ted in space a n d t ime. Despite be ing ext remely patchy resources , figs serve as keystone fruit resources in some, bu t no t all, t ropical forests (Gaut ier -Hion a n d Michaloud, 1989; Le igh ton a n d Leighton , 1983; T e r b o r g h , 1986). I am u n a w a r e of an ana logous example of a pant ropica l , spatio—temporally patchy flower source tha t serves as a keystone resource for nectar ivores.

Using publ i shed data , I have a t t empted to illustrate a bird's eye view of s p a t i o - t e m p o r a l variat ion in bird-visited fruit a n d flower species r ichness at two dif ferent spatial scales in F igure 3. In lowland Costa Rican wet forest, fruit diversity a p p e a r s to be somewhat bumpier (i.e., patchier?) t han flower diversity in t h r e e habitats at La Selva. Seasonal habitat shifts migh t be expec ted t h e r e , however , in bo th f rugivorous a n d nectar ivorous birds . Seasonal flower r ichness is h ighe r in bo th lowland a n d h igh land regions of Costa Rica t h a n at midd le elevations. Th i s creates a highly patchy landscape for h u m m i n g b i r d s a n d leads to the predic t ion that mid-elevation species should migra te e i ther ups lope or downslope at certain t imes of the year. G r a n t a n d G r a n t (1967: Fig. 2) il lustrate a similar seasonal shift in the location of h u m m i n g b i r d flowers in California; spr ing-b looming flowers a re concen t ra ted in the lowlands, whereas summer -b looming flowers a re concen t ra ted in the Sierra Nevada moun ta ins . Loiselle a n d Blake (1991a) also d o c u m e n t seasonal changes in fruit availability a long an al t i tudinal t ransect in Costa Rica.

Year- to-year variat ion in fruit a n d flower levels can also be substantial . In m e d i t e r r a n e a n scrublands , a n n u a l changes in fruit levels a re lower in the lowlands t h a n in the u p l a n d s ( H e r r e r a , 1984). Skeate (1987) no ted tha t annua l variat ion in fruit c rop size was lower in most species of bird-d ispersed shrubs , herbs , a n d vines t han in canopy trees in a n o r t h Florida h a m m o c k communi ty . Flower a n d nectar levels for h u m m i n g b i r d s , Aust ralian honeyea te r s , a n d Hawai ian honeycreepe r s somet imes show m a r k e d annua l variat ions; Aust ra l ian Eucalyptus is an especially variable flower source (Carpen te r , 1978; Keast, 1968; Paton, 1985a; Pyke, 1983, 1988; Stiles, 1978). Mast fruit ing, which is part icularly c o m m o n in West Malaysia ( A p p a n a h , 1985), is an e x t r e m e example of t empora l patchiness .


Because frugivores a n d nectar ivores interact mutualistically with their food plants , we can ask: T o what ex ten t a re pa t te rns of seasonal a n d spatial resource variat ion the p roduc t s of p l a n t - a n i m a l coevolution? H e r r e r a (1984), Skeate (1987), Snow (1971), a n d T h o m p s o n a n d Willson (1979), a m o n g o thers , have suggested tha t the fall—winter fruit ing peak in t emper ate lat i tudes is a response to b i rd migrat ion. As Rathcke a n d Lacey (1985) point out , however , d i sentangl ing cause a n d effect relat ionships in these systems can be difficult, a n d o the r explanat ions a re possible (e.g., H e r r e r a , 1984). Similarly, s taggered frui t ing a n d b looming seasons tha t p rov ide bi rds a n d m a m m a l s with spa t io - t empora l ly predictable food supplies have been in t e rp re t ed as p roduc t s of interspecific compet i t ion for l imited dispersers o r poll inators , bu t this hypothesis has se ldom been critically examined (Rathcke a n d Lacey, 1985; see Chap te r s 5, 11, a n d 13 for insect poll inator examples) . Stiles (1977, 1979) main ta ined that the s taggered b looming t imes of hummingb i rd -po l l i na t ed plants in Costa Rican wet forest a re the p r o d u c t of interspecific compet i t ion . In contrast , M u r r a y et al. (1987) failed to find the expec ted charac te r d isp lacement in the b looming times of two guilds of h u m m i n g b i r d flowers at Monteve rde , Costa Rica. T h e y a t t r ibu ted this lack of pa t t e rn to the s p a t i o - t e m p o r a l variat ion these plants exper ience in bo th plant—plant a n d plant—animal interact ions [but see Pleasants ' (1990) caveat o n the statistically conservative n a t u r e of thei r da ta analysis a n d C h a p t e r 13 for a discussion of identifying t rue guilds].

Despite the existence of controversy in this area , it seems reasonable to expect plants to evolve frui t ing a n d / o r flowering seasons tha t coincide with influxes of f rugivorous a n d nectar ivorous birds a n d m a m m a l s migra t ing n o r t h o r south to avoid physiologically (or biotically?) unfavorable conditions. Such evolut ion should p r o d u c e fruit o r nectar pathways. O n e possible example of such a pa thway is shown in F igure 4. La rge n u m b e r s of the nectar - feeding bat Leptonycteris curasoae migra te from tropical sou the rn Mexico to spend the sp r ing a n d s u m m e r in the Sonoran deser t of n o r t h e r n Mexico a n d the sou thwes te rn Uni ted States (Cockrum, 1989). D u r i n g thei r n o r t h w a r d migra t ion , they feed on nectar a n d pollen p r o d u c e d by several species of n igh t -b looming cacti. D u r i n g fall migra t ion, they feed on various species of n igh t -b looming Agave. Stable ca rbon isotope analysis of Leptonycteris muscle tissue confirms tha t this bat specializes on crassulacean acid metabol ism (CAM) plants (i.e., plants of the Cactaceae a n d Agavaceae) d u r i n g the spr ing, s u m m e r , a n d early fall, bu t not d u r i n g the winter w h e n it feeds on a mix tu re of C3 (e.g., tropical t rees a n d shrubs) a n d CAM plants (T. F leming a n d L. S te rnberg , unpub l i shed data , 1991). Such specialization increases the l ikelihood of coevolution be tween these bats a n d plants .

In summary , f rugivorous a n d nectar ivorous bi rds a n d m a m m a l s feed on food supplies that display considerable variat ion on a variety of t empora l a n d spatial scales. T h e availability of these foods appea r s to be patchier t han certain o the r kinds of foods. It is impor t an t to realize, however , tha t m u c h


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Figure 4 B l o o m i n g t imes a n d la t i tudinal d i s t r ibu t ions of bat- po l l ina ted cacti (filled rec tangles) a n d Agave ( o p e n rec tangles) in wes t e rn Mexico. G e n e r a of cacti i nc lude Carnegia (Carn . ) , Pachycereus (Pach.) a n d Stenocereus (Steno.) . Species of Agave i nc lude applanata, chrysantha, colorata, durangensis, flexispina, palmeri, shrevei, a n d wocomahi. F r o m G e n t r y (1982) , Sh reve a n d Wiggins (1964) .

of this patchiness is tempora l ly a n d spatially predictable . T h e s e animals d o not live in chaotic worlds such as depic ted in F igure I B . But ne i the r a re their worlds totally cons tan t (i.e., Fig. 1 A). T o cope with spa t io - t empora l ly inconstant, bu t con t ingen t (i.e., seasonally predic table ; Colwell, 1974) worlds, these animals should have spa t io - t empora l ly inconstant , bu t nonetheless predic table life histories.

III. Responses by Frugivores and Nectarivores to Resource Variability

A. Demographic Responses W e expect energetically expensive activities such as r e p r o d u c t i o n a n d molt to coincide with energetically favorable t imes of the year. Th i s is general ly the case in most species of frugivores a n d nectar ivores; b i r th a n d nest ing per iods t e n d to coincide with fruit a n d flower peaks, respectively. T w o well-s tudied neot ropica l species can be used to il lustrate this point .


Month Figure 5 T h e female r e p r o d u c t i v e cycle a n d popu l a t i on sex rat ios of t he f rug ivorous bat ,

Carollia perspicillata, in re la t ion to m o n t h l y fruit diversity a n d rainfall at San ta Rosa Nat iona l Park , Costa Rica. F r o m F leming (1988).

12. Resource Tracking in Frugivores and Nectarivores 3 6 7

Like most species of plant-visiting phyllostomid bats (Wilson, 1979), the short- tai led fruit bat (Carollia perspicillata) b reeds twice a year. Females give bi r th to a single y o u n g in the late d ry season (April), a n d in the midd le of the wet season (August) . Bi r th peaks coincide with two a n n u a l fruit peaks (Fig. 5), bu t the y o u n g a re no t weaned at equally favorable t imes of the year. Babies b o r n in Apri l become i n d e p e n d e n t (at abou t 5 weeks of age) w h e n fruit levels a r e increasing, whereas those b o r n in Augus t become in d ep en d e n t after the wet-season fruit peak. Surprisingly, survivorship differences be tween these two cohor ts of y o u n g d o not differ significantly (Fleming, 1988).

An u n u s u a l aspect of the d e m o g r a p h y of Carollia, at least in Costa Rican lowland d ry tropical forest, is that most females, bu t no t males, migra te from thei r wet-season cave roosts d u r i n g the d ry season w h e n fruit levels general ly a r e low. As a result , sex ratios in these caves become strongly male-skewed late in the d ry season (Fig. 5), a n d most males in these caves par t ic ipate in only one mat ing per iod pe r year. W h e n they r e t u r n to the lowland caves in the wet season, females a re p r e g n a n t with babies fa thered in thei r ( u n k n o w n bu t probably mon tane ) d ry season roosts. W h e n they arr ive in thei r dry-season roosts, they a re p r e g n a n t with babies fa thered in their wet-season roosts. In this species, females apparen t ly migra te for energet ic reasons , a n d males a re sedentary for social reasons (Fleming, 1988).

T h e long-tailed he rmi t (Phaethornis superciliosus) is one of the most comm o n h u m m i n g b i r d s in the unde r s to ry of lowland wet forests in Costa Rica. Phaethornis is a lek-breeding species whose annua l reproduc t ive cycle is summar i zed in F igure 6. T h e main calling a n d nest ing season occurs in J a n u a r y t h r o u g h Ju ly w h e n nec tar levels, especially those of its main food plant Heliconia pogonatha, a re highest . Stiles a n d Wolf (1979) est imate that u p to 7 5 % of the a n n u a l mortal i ty in this species occurs d u r i n g October a n d N o v e m b e r w h e n flowers a re scarcest. T h e y suggest that this species may be food l imited at thei r La Selva study site.

Many o t h e r studies indicate that b r eed ing activity a n d resource levels a re positively cor re la ted in frugivores a n d nectar ivores. In frugivores, b i r th peaks in New Wor ld pr imates (e.g., Ateles, Saimiri, a n d Saguinus) coincide with fruit peaks ( T e r b o r g h , 1983; van Roosmalen, 1980), as d o the b r e e d i n g seasons of manak ins (Manacus, Pipra) [ (on B a r r o Colorado , bu t possibly no t at La Selva; cf. W o r t h i n g t o n (1982) a n d Levey (1988)] , a n d of the resplend e n t quetzal (for the scientific names of b i rds men t ioned in the text, see the Append ix ) (Wheelwright , 1983). T h e reproduc t ive cycles of t h ree species of f rugivorous bats (Artibeus jamaicensis, Eidolon helvum, a n d Haplonycteris fis-cheri) a r e unusua l a m o n g bats because they involve delayed implanta t ion o r delayed embryonic deve lopment . H e i d e m a n (1988) a n d Sandell (1990) hypothesize that these reproduc t ive cycles have evolved to allow both ma t ing a n d bi r ths to coincide with energetically favorable t imes of the year. In

Figure 6 T h e m a l e cal l ing a n d female b r e e d i n g season of t he long-tai led h e r m i t h u m m i n g b i r d (Phaethornis superciliosus) in re la t ion to m o n t h l y flower diversi ty a n d rainfall at La Selva, Costa Rica. F r o m Stiles a n d Wolf (1979).


nectar ivores , b r e e d i n g - f l o w e r peak correlat ions have been r e p o r t e d for Aust ra l ian honeyea te r s (Paton, 1985b; Pyke, 1983; Pyke a n d Recher , 1986) a n d New Wor ld h u m m i n g b i r d s (Stiles, 1973, 1980, 1985b).

In add i t ion to inf luencing the t iming of b reed ing , fruit a n d nectar levels d e t e r m i n e pa t t e rns of f rugivore a n d nectar ivore a b u n d a n c e . A l though they a re se ldom m e a s u r e d s imultaneously in the same study area , it is likely that the a n n u a l (and often ins tantaneous) biomass of fruit is far g rea te r t h a n that of nec ta r (and insects?). For example , at peak frui t ing t imes the wet-weight biomass of 14 species of bat-dispersed fruits in Costa Rican d ry tropical forest r anges f rom 0.1 to 42 k g / h a / d a y with a m e d i a n value of 1.5 k g / h a / day. T h i s can be c o m p a r e d with values of 0.01 to 0.11 k g / h a / d a y of nec tar in t h r e e species of bat-pol l inated c o l u m n a r cacti in the Sono ran deser t , whose ba t - f lower densi ty is m u c h h ighe r t han that of tropical d ry forest (Fleming, 1988; T . F leming a n d P. H o r n e r , unpub l i shed data, 1990). Similar meas u r e m e n t s for insect biomass would be ext remely valuable.

T h e s e kinds of biomass differences m e a n that frugivores should have h ighe r popu la t ion densit ies, on average , t han nectar ivores a n d insectivores. In s u p p o r t of this expecta t ion, T e r b o r g h et al. (1990) r e p o r t e d tha t a rborea l f rugivore biomass at M a n u Nat ional Park, Peru , was two o r d e r s of magni t u d e h ighe r t h a n tha t of nectar ivores (26 kg /100 ha, cf. 0.2 kg /100 ha) . Mist-net cap tu res of bats at several neotropical locations indicate that fru-givorous species of the phyl lostomid subfamilies Caroll i inae a n d S tenoder -ma t inae a r e 4 - 5 t imes m o r e a b u n d a n t than nectar ivorous Glossophaginae a n d insectivorous Phyl lostominae (Fleming, 1988). A similar a b u n d a n c e dispari ty occurs a m o n g frugivorous a n d insectivorous bi rds in m e d i t e r r e a n scrubland ( H e r r e r a , 1984) a n d tropical habitats (Karr , 1990; Loiselle, 1988; Loiselle a n d Blake, 1991a).

A second resource- re la ted pa t t e rn is t empora l variations in a b u n d a n c e , which a re often g rea te r in frugivores a n d nectar ivores than in insectivores. Such differences have been r e p o r t e d for t e m p e r a t e frui t-eat ing bi rds (Mart in a n d Karr , 1986b) a n d for Austra l ian honeyea te rs (Newland a n d Wooller , 1985; Ramsey, 1989) (Fig. 7). As I shall discuss in detail , these differences often resul t f rom the g rea te r seasonal mobility of frugivores a n d nectar ivores c o m p a r e d with that of insectivores.

A th i rd pa t t e rn is seasonal changes in frugivore a n d nectar ivore abundance , which often corre la te with seasonal changes in fruit a n d flower abu ndance s . Positive re la t ionships be tween a b u n d a n c e a n d resource levels have been r e p o r t e d in t e m p e r a t e a n d tropical f rugivorous bi rds (Blake a n d H o p p e s , 1986; Levey, 1988; Loiselle, 1988; Loiselle a n d Blake, 1991a; Mar t in a n d Kar r , 1986b), in tropical h u m m i n g b i r d s (Feinsinger, 1976, 1980; Lyon, 1976; Stiles, 1980, 1985b), a n d in Austra l ian honeyea te rs (Collins, 1980; Collins a n d Briffa, 1982; McFar land , 1986; Paton, 1985b; Pyke, 1985; Ramsey, 1989). Again, m u c h of this variat ion in a b u n d a n c e can be a t t r ibuted to immigra t ion r a t h e r t han to r ep roduc t ion a n d mortali ty.



Month Figure 7 M e a n n u m b e r ( ± 1 S.E.) of h o n e y e a t e r s a n d insect ivorous b i rds seen in m o n t h l y

t ransects in Banksia w o o d l a n d s n e a r Pe r th , Aust ra l ia . R e d r a w n with pe rmiss ion f rom Ramsey (1989).

B. Movements As Kar r (1990) no ted for bi rds , the t racking of food resource a b u n d a n c e drives m u c h of the daily a n d seasonal movement , including habitat shifts and al t i tudinal a n d lat i tudinal migrat ions , of frugivores a n d nectar ivores. T h e impor t ance of p lant resources in de t e rmin ing movement s in nectarivorous birds is h ighl ighted in the following quotes , "nectar ivorous birds as a g r o u p show m o r e p r o n o u n c e d migra tory o r nomadic behavior than d o birds of virtually any o t h e r t rophic category" (Stiles, 1980, p . 340). " T h e overwhe lming majority of seasonal movemen t s in the Mel iphagidae [honeyeaters] a re directly associated with nectar feeding" (Keast, 1968, p . 198).

1. Daily Movements How far d o frugivores a n d nectar ivores r ange on a daily basis to harvest their food? In pr imates , body size a n d food habits interact to d e t e r m i n e daily r ange lengths . For example , because they are relatively large a n d specialize on r ipe fruits, sp ider monkeys (Ateles) have larger daily r a n g e lengths (up to 5 km) than d o smaller Saimiri and Cebus monkeys (up to 3 to


4 km), o r la rger bu t m o r e folivorous Lagothrix a n d Brachyteles monkeys (up to 1.6 km) (Robinson a n d J anson , 1987). Similarly, two sympatr ic hylo-batids, t he larger , m o r e folivorous s iamang (Hylobates syndactylies), a n d the m o r e f rugivorous lar g ibbon (H. lar), differ in daily r a n g e length a n d feeding t ime; the lar travels twice as far bu t feeds for only 6 9 % as long as the s iamang (Oates, 1987). Waser (1987) no ted that a large patch specialist pr ima te has evolved to harvest e p h e m e r a l bu t s u p e r a b u n d a n t fruits (e.g., figs) on each tropical cont inent . Each of these pr imates (Hylobates, Pongo, Pan, Cercocebus, a n d Ateles) has e n o r m o u s ranges for harves t ing these fruits.

Daily r a n g e lengths of f rugivorous bi rds a n d bats can also be substantial . Forag ing movemen t s of tropical unde r s to ry frugivores, such as manak ins a n d o the r small passer ines a n d Carollia bats, vary from a few h u n d r e d mete rs to 3 k m (Fleming, 1988; Murray , 1988; Snow 1962a,b). In contrast , canopy feeders such as oilbirds, fruit p igeons, birds of paradise , a n d p te ro-pod id fruit bats r a n g e m u c h m o r e widely (i.e., 1 0 - 5 0 km) be tween roosts a n d feeding areas (Beehler a n d Pruet t - Jones , 1983; Bradbury , 1977; Fleming, 1982; Le igh ton a n d Leighton, 1983; Snow, 1962c). T e r b o r g h et al. (1990) r e p o r t e d tha t flocks of canopy-feeding frugivorous bi rds have m u c h la rger ter r i tor ies ( > 2 0 ha) a n d use the forest in a patchier fashion t han d o unde r s to ry flocks whose terr i tor ies average about 5 ha. Some ch i rop te ran fig specialists (e.g., Artibeus, Nyctimene) forage only a few h u n d r e d mete r s f rom the i r day roosts when fruit ing p lant densities a re h igh (Morr ison, 1978; Spence r a n d Fleming, 1989), whereas o thers (e.g., Hypsignathus, Ptero-pus) fly 5 - 5 0 km from thei r roosts to feed (Bradbury , 1977; Marshall , 1985). T h e low density of fig t rees in Gabon forests prec ludes pr imates a n d large bi rds f rom specializing on them. Ins tead , figs a re ea ten by wide- ranging p t e r o p o d i d bats (Gaut ie r -Hion a n d Michaloud, 1989).

T h e daily foraging ranges of nectar - feeding birds a n d m a m m a l s a re less well s tudied t han a re those of fruit-eaters. Ter r i to r ia l h u m m i n g b i r d s a n d honeyea te r s appa ren t ly move relatively shor t distances (up to 1 km from their terr i tories) to feed, whereas t rap- l iners , such as the long-tailed hermi t , probably a re m o r e mobile (Linhart , 1973; Newland a n d Wooller , 1985; Paton, 1985b; Stiles, 1973; Stiles a n d Wolf, 1979). T h e nightly c o m m u t e distances be tween roosts a n d feeding areas of nectar ivorous bats r a n g e f rom shor t (probably < 5 km in Glossophaga) to relatively long ( 1 0 - 3 0 km in Anoura, Eonycteris, a n d Leptonycteris) (Helversen a n d Reyer, 1984; P. H o r n e r a n d T . Fleming, unpub l i shed data , 1990; Lemke , 1984; Start a n d Marshall , 1976). Radio- t racking studies of Leptonycteris curasoae in the Sonoran deser t indicate tha t these 27 g bats rout inely fly 8 0 - 1 0 0 km d u r i n g a 7-hr foraging pe r iod (P. H o r n e r a n d T . Fleming, unpub l i shed data , 1990).

2. Seasonal Movements Seasonal movemen t s of varying spatial magn i tudes a re c o m m o n in frugivores a n d nectar ivores . T h e s e movemen t s can be b r o k e n d o w n into t h r ee


classes based on spatial scale: habi tat shifts, al t i tudinal migrat ions , a n d lat i tudinal migra t ions . Habi ta t shifts a p p e a r to be widespread in plant-visiting b i rds a n d mammal s . In the tropics, such shifts generally involve movemen t s a m o n g habitats a long successional gradients (Karr , 1989, 1990). For example , Levey (1988) r e p o r t e d tha t res ident f rugivorous bi rds at La Selva, Costa Rica, moved from pr imary forest into second growth when fruit levels in the fo rmer habi tat decl ined relative to those in the latter. Resident h u m m i n g b i r d s at tha t site also exhibit food-related habitat shifts (Stiles, 1980). In central Panama , f rugivorous birds a p p e a r to be m o r e likely to change habitats t han insectivores o r nectar ivores (Mart in a n d Karr , 1986a). Many species of Austra l ian honeyea te rs u n d e r g o habitat changes as they track chang ing flower dis t r ibut ions (Ford, 1985; Keast, 1968; Paton, 1985a; Pyke, 1983, 1985). A l t h o u g h resource t racking appea r s to be a major motivat ing factor beh ind these habi tat shifts, o the r factors, inc luding seasonal microclimatic constra ints a n d nest ing r equ i r emen t s , can also influence these movemen t s (Karr a n d Brawn, 1990; Skutch, 1950).

Alt i tudinal migra t ions have been best s tudied in Costa Rican bi rds in which frugivores a n d nectar ivores a re m o r e likely to move ups lope o r downs lope t han a re insectivores (Stiles, 1983). T h e t iming of these movements , which general ly occur outs ide the b r eed in g season, differs a m o n g frugivores a n d nectar ivores . Frug ivorous al t i tudinal migran ts arr ive in the lowlands in October a n d N o v e m b e r a n d r e t u r n ups lope in J a n u a r y ; h u m mingb i rds arr ive in the lowlands be tween Apri l a n d Augus t a n d begin to r e t u r n ups lope in Augus t . Arrivals in the lowlands coincide with per iods of h igh fruit o r flower a b u n d a n c e (Blake et al, 1990). Migrat ion tendencies in f rugivorous b i rds a re complex , a n d Loiselle a n d Blake (1991b) identify t h r ee classes of al t i tudinal migran ts :

1. comple te long dis tance migrants—species whose en t i re popula t ions move > 1000 m in elevation between b r eed in g a n d n o n b r e e d i n g sites;

2. comple te shor t -dis tance migran ts moving < 1000 m in elevation be tween b r ee d ing a n d n o n b r e e d i n g sites; a n d

3. part ial short-dis tance migrants—species in which only a por t ion of the popu la t ion leaves the b r e e d i n g site.

T h e y also no ted that the p r o p o r t i o n of mig ran t species a n d migran t individuals increases with increasing elevation, a n d that the intensity a n d t iming of migra t ions vary be tween years.

Lat i tudinal migran t s a b o u n d a m o n g N o r t h T e m p e r a t e zone birds a n d bats, inc luding all avian nectar ivores a n d frugivores. H u m m i n g b i r d s b r ee d ing in western N o r t h Amer ica a n d migra t ing south a long the Sierra Nevadas move in waves a n d par t i t ion limited flower resources inter- a n d intraspecifically by m e a n s of different migra t ion times (Carpen te r , 1978; Kodr ic-Brown a n d Brown, 1978; Phillips, 1975). U p o n arrival at their win te r ing g r o u n d s in Mexico a n d Cent ra l America , these species a re socially


subord ina te to res ident tropical species (DesGranges and Gran t , 1980; Wolf, 1970). Partially or wholly frugivorous lat i tudinal migran ts become i m p o r t a n t c o m p o n e n t s of winter b i rd communi t ies in the Cent ra l Amer ican tropics, as well as in m e d i t e r r a n e a n scrublands (He r r e r a , 1984; Levey, 1988).

C o m p a r e d with birds , less is known about lat i tudinal migra t ions in plant-visiting bats. In the New Wor ld , long-distance migra t ions a p p e a r to occur only in nec tar ivorous bats associated with the Sonoran deser t (Leptonycteris a n d Choeronycteris) (Barbour a n d Davis, 1969). It is likely, however , that o the r neotropical p h y t o p h a g o u s bats (e.g., Phyllostomus discolor) u n d e r g o at least shor t -dis tance seasonal movemen t s (Hei thaus et al, 1975). T h r e e West African f rugivorous bats {Eidolon helvum, Myonycteris torquata, a n d Nanonyc-teris veldkampi) migra te f rom the forest zone n o r t h to the savanna zone early in the wet season. T h o m a s (1983) postula ted that these species migra te against a food-resource gradien t , away from an e n v i r o n m e n t rich in fruit a n d compet i tors , to one in which food a n d compet i t ion levels a re lower because of s t ronger seasonal food fluctuations. Pteropus bats in eas tern Austral ia also migra te h u n d r e d s of ki lometers , bu t not necessarily in a lat i tudinal fashion, to d i f ferent feeding areas a n d roost sites in response to changes in the locations of good flower sources (Nelson, 1965; Ratcliffe, 1932).

In addi t ion to habitat , al t i tudinal , a n d lat i tudinal shifts, apparen t ly nomadic wande r ings a re known to occur in some species of nectar ivorous a n d frugivorous bi rds a n d mammals . Keast (1968), for example , r e p o r t e d that abou t 2 3 % of Aust ra l ian bird species u n d e r g o r a n d o m , nomadic , o r o ther wise spatially nonrepe t i t ive movement s , whereas only abou t 8% of the species u n d e r g o a n n u a l n o r t h - s o u t h movement s . H e no ted tha t in honeyeaters t he r e is a b r o a d correla t ion be tween the p ropor t i on of species mak ing seasonal movemen t s in an area a n d the variability of that area 's rainfall; 39% of 65 species m a k e modera te ly to strongly deve loped nomad ic movements . In Aust ra l ian eucalypt forests, b i rds such as honeyeaters , lorikeets, a n d parda lo tes feeding on nectar , m a n n a , honeydew, or lerps a re often nomadic , whereas insectivores are sedentary (Ford, 1985). T h e smallest of Australia 's four species of flying foxes (Pteropus scapulatus) is s trongly d e p e n d e n t o n Eucalyptus flowers a n d is the most nomad ic species (Richards, 1983a). A n u m b e r of Old Wor ld f rugivorous birds , inc luding fruit p igeons in Austral ia a n d Borneo , a n d flowerpeckers a n d birds of paradise in New Guinea , a re also t h o u g h t to be nomad ic (Crome, 1975; Leighton a n d Leighton, 1983; Pra t t a n d Stiles, 1985).

As Stiles (1973, 1980) has no ted , t e m p e r a t e and tropical h u m m i n g b i r d s can be highly nomadic . Trop ica l h u m m i n g b i r d communi t ies contain t h r ee major g r o u p s of species: (1) res idents that t end to de fend the richest nectar sources , (2) al t i tudinal o r la t i tudinal migran ts , a n d (3) w a n d e r e r s o r n o m a d s tha t follow the b looming seasons of par t icular species from one habitat to


a n o t h e r (DesGranges a n d Grant , 1980; Feinsinger, 1976, 1980; Stiles, 1980, 1985b). T h r e e of the 14 species of h u m m i n g b i r d s feeding in successional habitats at Monteve rde , Costa Rica (ca. 1500 m) are n o m a d s ; an addi t ional five species a re al t i tudinal migran ts ; a n d the r ema in ing species a re e i ther residents (four species), o r migran ts from adjacent habitats (Feinsinger, 1976). T h e ebb a n d flow of h u m m i n g b i r d species into and ou t of par t icular habitats thus make their communi t i es extremely dynamic .

C. Social Responses 1. Spacing Patterns Many au tho r s (e.g., W r a n g h a m , 1987) have pointed out that the economic defendabil i ty a n d s p a t i o - t e m p o r a l dis tr ibut ion of food, a long with p re dat ion p ressure , a re major factors influencing the evolution of socially med ia ted spacing pa t t e rns in animals . As illustrated in Figure 8, different kinds of spacing pa t te rns o r social organizat ions will be favored, d e p e n d i n g on the dis t r ibut ion a n d defendabil i ty of food in space a n d t ime. At one e n d of this defense—cost c o n t i n u u m are aggressive intra- and interspecific terr itorial systems associated with resources that a re relatively uniformly distribu ted in space. At the o t h e r e n d a re nomadic flocks associated with widely

o

Nomadism

Flocks

Home Range T e r r i t o r i a l i t y

L o w

R e s o u r c e A g g r e g a t i o n or

H i g h

U n p r e d i c t a b i l i t y

Figure 8 T h e gene ra l r e la t ionsh ip be tween the cost of r e sou rce de fense , r e sou rce aggrega t ion o r unpred ic tab i l i ty , a n d spatially def ined social o rgan iza t ion . R e d r a w n with permiss ion f rom Wiens (1976).


spaced resource patches . Spacing pa t te rns in frugivores a n d nectar ivores a p p e a r to be sensitive to food distr ibutions. In general , nectar ivores t end to occur at the aggressive end , a n d frugivores t end to occur at t he gregar ious e n d of this c o n t i n u u m . Accord ing to my second hypothesis (page 357), insectivores should exhibit terr i torial behavior m o r e frequent ly t han d o e i ther frugivores or nectar ivores .

a. Patterns in Frugivores Stiles' (1983) review of the social systems of Costa Rican b i rds provides an excellent overview of the influence of diet on tropical avian spacing pa t te rns . D u r i n g the n o n b r e e d i n g season, most t ropical frugivores a re nonter r i tor ia l , whereas insectivores t end to main ta in terr i tor ies yea r - round . At all elevations, the moda l social system of avian frugivores is single-species flocks, bu t mixed-species flocks of frugivores a re also c o m m o n (Buskirk, 1976; Mor ton , 1979; M u n n , 1985; Powell, 1985; Remsen , 1985). Flocking is m o r e c o m m o n in canopy frugivores (e.g., araca-ris, tanagers) t h a n in unde r s to ry frugivores (e.g., manakins , cer tain tana-gers a n d flycatchers), in pa r t because of the the larger pa tch sizes a n d grea te r in te rpa tch distances of canopy fruits. C o m p a r e d with mixed-species flocks of insectivores, the foraging locations of tropical frugivores in mixed-species flocks over lap extensively, d o m i n a n c e hierarchies a r e absent , a n d flocks a re less likely to be terr i torial (Munn , 1985; Powell, 1985). In contrast , t e m p e r a t e zone avian frugivores a n d t e m p e r a t e migrants in the tropics t end to be solitary foragers (He r r e r a , 1984; Stiles, 1983). A m o n g overwinter ing frugivores in south Florida, gray catbirds a n d white-eyed vireos a re solitary foragers , whereas Amer ican robins a n d t ree swallows forage in intraspecific flocks (personal observat ion, 1990).

Spacing pa t t e rns in New Guinea bi rds of paradise also differ a m o n g diet classes. Forag ing terr i tor ies occur in the insectivorous buff-tailed sicklebill, whereas ove r l app ing a n d n o n d e f e n d e d foraging ranges occur in frugivorous species (e.g., magnificent a n d raggiana birds of paradise , t r u m p e t manucodes ) (Beehler , 1987). Flocking behavior does no t occur in this family.

Aggressive interact ions a m o n g avian frugivores feeding in the same t ree t end to be in f requen t and , w h e n present , t end to be di rected toward conspe-cifics r a t h e r t han heterospecifics (e.g., Cruz , 1974; F leming a n d Williams, 1990; Leek, 1969). Ter r i to r ia l defense of individual fruit ing trees, however , has been observed in mistle th rushes in Britain (Snow a n d Snow, 1984), a n d in four species of New Guinea forest birds (Pratt, 1984)

Most f rugivorous bats roost gregariously by day bu t feed solitarily a n d nonterr i tor ia l ly at night . In contrast , some, bu t not all, t ropical insectivorous bats de fend feeding terr i tor ies at n ight (Bradbury a n d E m m o n s , 1974; B r a d b u r y a n d V e h r e n c a m p , 1976; Fen ton and Rau tenbach , 1986; Vaug-han , 1976; V a u g h a n a n d V a u g h a n , 1986). T h e feeding behavior of most frugivorous phyl lostomid bats generally prec ludes defense of fruit ing trees


or areas conta in ing fruit ing trees. As described in detail in Bonaccorso and Gush (1987), F leming (1988), a n d Morr i son (1978), this behavior includes harves t ing o n e fruit o r par t of a fruit at a t ime a n d taking it to a secluded night roost to consume . T h e s e bats usually sleep in their n ight roost when not eat ing. Large n u m b e r s of f rugivorous bats often congrega te in large fruit ing trees (e.g., figs) bu t en te r a n d leave these trees singly r a the r than in flocks (e.g., Augus t , 1981; Morr ison, 1978). In contrast , Pteropus bats often travel f rom their day roosts to their feeding areas in flocks. Once they arrive at frui t ing or flowering t rees , however , they sometimes set u p individual terr i tor ies of a few square mete r s in the t ree crown (G. Richards , personal communica t ion , 1987; persona l observat ion, 1987).

Frug ivorous pr imates show a wide r ange of spacing pa t te rns , which are influenced by food dis t r ibut ions a n d mat ing systems. Terr i tor ial i ty is widesp read in p r imates a n d somet imes reflects the economic defendabili ty of food (Oates, 1987). For example , at M a n u National Park a n d elsewhere in Peru , two species of t amar ins (either Saguinus imperator o r mystax a n d S. fuscicollis) travel in mixed-species g roups , feed on synchronously fruit ing plants bea r ing small n u m b e r s of r ipe fruit daily, a n d de fend relatively small

0 1 i ' i i ' i i I 1 S O N D J F M A M J J A

Month Figure 9 Mon th ly c h a n g e s in t he fo rag ing-pa r ty size of black spicier m o n k e y s (Ateles

paniscus) a n d r e s o u r c e - p a t c h size, m e a s u r e d as t he total basal a r ea of t rees a n d lianas b e a r i n g m a m m a l - d i s p e r s e d fruits, at M a n u Nat iona l Park , Pe ru . R e d r a w n with pe rmiss ion f rom Syming ton (1988).

12. Resource Tracking in Frugivores and Nectarivores 3 7 7

terr i tor ies against o the r t amar in g roups (Garber , 1988; T e r b o r g h , 1983). In contrast , squirre l monkeys (Saimiri sciureus) at M a n u feed on figs, which are supe r a b u n d a n t bu t e p h e m e r a l resources , a n d travel in large g ro u p s whose ranges over lap a n d a re no t de fended . In genera l , f rugivorous pr imates that a re m o n o g a m o u s , o r that possess small h o m e ranges which can be patrol led daily, a re usually terr i tor ial , whereas those with large over lapp ing ranges a re not (Cheney, 1987).

G r o u p sizes in g regar ious pr imates t end to be corre la ted with resource patch size. At Santa Rosa Nat ional Park in Costa Rica, for example , the social systems of howler (Allouatta palliata) a n d sp ider (Ateles geoffroyi) monkeys can be descr ibed as fusion-fission because g roups coalesce, o r split u p , d e p e n d ing o n the sizes of fruit c rops at di f ferent t imes of the year ( C h a p m a n , 1988). In sp ider monkeys (A. paniscus) at Manu , foraging-par ty size tracks food-patch size (Fig. 9). Aggressive behavior a n d compet i t ion for food act to adjust g r o u p size to food-patch size (Symington, 1988). Foraging-par ty sizes t end to be la rger in the bonobo (Pan paniscus), which feeds in larger t rees, t han in the ch impanzee (P. troglodytes) (White a n d W r a n g h a m , 1988). G r o u p cohesiveness a n d ra te of m o v e m e n t differs greatly be tween pr imates that feed on low-density insects o r fruit [foragers in Oates ' (1987) te rminology] , c o m p a r e d with those feeding on highly c lumped fruits (banqueters).

b. Patterns in Nectarivores Aggressive defense of nectar resources is c o m m o n in all families of nectar ivorous birds (Stiles, 1973; Gill a n d Wolf, 1975; Pyke, 1980). It is especially c o m m o n in h u m m i n g b i r d s , bo th d u r i n g a n d outs ide of the b r e e d i n g season. Many studies (reviewed in Feinsinger , 1987) have shown tha t h u m m i n g b i r d s a re remarkably flexible in (1) their ability to t u r n terr i tor ial behavior on a n d off in response to resource levels, a n d in (2) adjust ing terr i tory size to c u r r e n t nectar densit ies. C a r p e n t e r (1987) points ou t tha t h u m m i n g b i r d s t end to de fend food terr i tor ies only when regional food levels a re low, even w h e n local food levels a re high. She a rgues tha t h igh mobility has been selected for in nectar ivores to assess regional as well as local food levels before dec id ing w h e t h e r o r no t to de fend a ter r i tory . Hawai ian honeycreepe r s (Drepanid idae) a re also less likely to de fend terr i tor ies in years when flower densit ies are low (Carpen te r , 1978).

Ter r i to r ia l behavior is not universal in tropical h u m m i n g b i r d s . Stiles (1983) indicates that lowland h u m m i n g b i r d s have two moda l foraging (and social) systems:

1. in socially d o m i n a n t species, which are usually straight-billed, have h igh wing-disc loading, bu t a re not necessarily large, males de fend c lumps of flowers against conspecific males a n d heterospecifics; a n d

2. in socially subord ina te species, which include hermi t s a n d short-billed species with low wing-disc loading, birds e i ther forage a long trap lines of widely spaced plants (hermits) , steal nectar f rom d e f e n d e d patches , o r visit flowers no t used by d o m i n a n t species.


In h u m m i n g b i r d communi t ies in Colima, Mexico, mig ran t species a re m o r e likely to set u p terr i tor ies than a re res ident a n d wanderer species (Des-Granges a n d Gran t , 1980). Only four of six species a re terr i torial d u r i n g the s u m m e r m o n t h s in m o n t a n e meadows in Mexico (Lyon, 1976), whereas all four co-occuring species de fend certain flowers at par t icular t imes of the year in a m o n t a n e communi ty in Costa Rica (Wolf et al, 1976). Finally, flocking behavior is u n r e p o r t e d in h u m m i n g b i r d s except d u r i n g per iods of migra t ion , a n d then only in certain species (e.g., Calypte anna) (Stiles, 1973).

Ter r i to r ia l behavior appea r s to be less c o m m o n , a n d flocking behavior , m o r e c o m m o n in Austra l ian honeyea te rs t han in h u m m i n g b i r d s . Pyke (1980) suggested that this is because flower densities a re p e r h a p s h igher , on average, a n d p reda t ion risks, lower for h u m m i n g b i r d s t han for honey-eaters . T h e presence of territoriali ty in honeyea te rs has been r e p o r t e d by Ford a n d Paton (1977), Newland a n d Wooller (1985), a n d Paton (1985a,b), a n d its absence by C a r p e n t e r (1978), a n d Collins a n d Briffa (1982). In t raspecific flocking, which allows birds to find a n d p r e e m p t c lumped flower resources , occurs in yellow-faced, whi te-naped, a n d scarlet honeyeaters (McFarland, 1986).

Size-based interspecific d o m i n a n c e relat ionships somet imes d e t e r m i n e access to flowers in honeyea te r communi t ies (McFarland, 1986; Newland a n d Wooller , 1985). Because of their large size, watt lebirds (Anthchaera) a re generally able to control access to rich flower patches except against flocks of small silvereyes (Zosterops). Watt lebirds thus often occur at the rich e n d of nectar resource gradients , whereas small subord ina te species (e.g., spinebills (Acanthorhynchus)) a re often re legated to the low e n d of such gradients . Medium-sized honeyea te r s (e.g., New Hol land honeyeaters) a re often m o r e constant in thei r p resence in honeyea te r communi t ies than a re la rger o r smaller species, because they can profitably forage at c l umped as well as at d ispersed nectar sources (Paton, 1985b). Watt lebirds need rich c lumps to forage profitably, whereas small spinebills often migra te to r icher resource areas despi te be ing able to persist in areas when resource levels a re low.

Ter r i to r ia l behavior appea r s to be less c o m m o n in nectar ivorous bats than it is in bi rds . L e m k e (1984) r e p o r t e d that in Colombia Glossophaga soricina defends flowers of Agave desmettiana against conspecifics in the early hou r s of the evening, before visiting o the r flowers in t rap-l ine fashion. It is likely that the small p t e r o p o d i d Syconycteris australis is a persis tent de f ende r of Banksia a n d o the r flowers in eas tern Australia (G. Pyke a n d D. Woodside , personal communica t ion , 1987; Richards , 1983b). Gould (1978) no ted that individuals of Pteropus vampyrus de fend par ts of the canopy of flowering Durio zibenthus t rees against conspecifics, a n d suggested that Eonycteris spelea also de fends Parkia speciosa flowers in Malaya. Defense of flowers has not been observed in o the r species of flower-visiting bats.

O t h e r t han Lemke 's (1984) study, t rap-l ine foraging behavior — t h e usual foraging m e t h o d in he rmi t h u m m i n g b i r d s — h a s not been directly observed in nectar ivorous bats, t h o u g h its suspected occur rence has been men t ioned


by Baker (1973), He i thaus et al (1974), and Gould (1978). Flock foraging has been be t t e r -documen ted in nectar ivorous bats. It occurs in Leptonycteris curasoae a n d Phyllostomus discolor in the New Wor ld a n d in Epomophorous gambianus in Africa, a n d Eonycteris spelea in Malaya (Fleming, 1982). G r o u p size in Leptonycteris a n d Phyllostomus appea r s to be re la ted to flower density. For example , w h e n they visit individual flowers of the cactus Pachycereus pringlei, g r o u p s of Leptonycteris contain 2 - 5 bats, whereas they contain 20 or m o r e individuals at panicles of Agave palmeri flowers (P. H o r n e r a n d T . Fleming, unpub l i shed da ta , 1990; Howell , 1979).

Nectar is an u n c o m m o n dietary i tem in pr imates a n d o the r a rborea l mammals . Cer ta in terr i tor ial species of noc turna l pros imians as well as d iu rna l species of cebids a n d callitrichids a re known to consume nectar , especially d u r i n g tropical d ry seasons (Garber , 1988; Hladik et al, 1980; J a n s o n et al, 1981; T e r b o r g h a n d Stern, 1987). G r o u p s of saddle-backed tamar ins (Saguinus fusicollis) visit Combretum, Quararibea, a n d Symphonia flowers in t rap- l ine fashion. T rap - l in ing has also been observed in noc tu rna l species, such as the marsupia l Didelphis marsupialis, a n d the procyonids Potos flavus a n d Bassaricyon alleni visiting Quararibea flowers in Peru , bu t no t in the marsup ia l Caluromysiops irrupta a n d the n ight monkey (Aotus trivirgatus) ( J a n s o n et al, 1981).

2. Mating Patterns Because resource dis t r ibut ions d e t e r m i n e , in par t , the polygyny potential of any e n v i r o n m e n t , they can play an i m p o r t a n t role in the evolut ion of avian a n d m a m m a l i a n ma t ing systems (Emlen a n d Or ing , 1977). Env i ronmen t s will have h igh polygyny potent ia l wheneve r resources a re d is t r ibuted in de fendab le c lumps tha t at t ract several potent ia l mates . A l though most fruit-o r nectar -ea t ing b i rds a n d m a m m a l s confo rm to the moda l mat ing systems of thei r classes (monogamy a n d polygamy, respectively), some species differ in spectacular fashion f rom expected ma t ing systems. While no t exclusively restr icted to f rugivorous a n d nectar ivorous species, lek ma t ing systems a re m o r e c o m m o n in these diet classes t h a n in o thers , a n d it seems reasonable to postulate tha t this association is not for tui tous. In some g ro u p s of b i rds a n d mammals , feeding on fruits o r nectar has favored the evolut ion of lek mat ing .

a. Patterns in Frugivores Snow (1971 , p . 198) was the first orni thologis t to poin t ou t the association be tween frugivory and lek ma t ing in tropical forest b i rds :

H e n c e it m a y be e x p e c t e d o n theore t ica l g r o u n d s tha t fruit will cons t i tu te , at t h e seasons w h e n it is available, a n a b u n d a n t food supp ly a n d o n e which is easily ob t a ined , w h e r e a s insects will cons t i tu te a less a b u n d a n t food supp ly a n d o n e which is less easily located. It is surely for this r ea son tha t lek behav iou r , which entails the p r e s e n c e o f t h e d i sp lay ing b i rds o n the i r d isplay p e r c h e s for t he g r e a t e r p a r t of t h e day, has evolved in s o m e g r o u p s of f rug ivorous t ropica l forest b i rds , b u t no t in insect ivorous b i rds .


A m o n g frugivorous birds , lek ma t ing is found in neotropical manakins , cotingids, a n d certain flycatchers and , in the paleotropics, in certain birds of paradise .

Male emancipa t ion f rom nest ing dut ies is a key step in the evolution of lek mat ing in b i rds . Male emancipa t ion will be permitted when females can easily find food (usually fruit) for themselves, a n d can feed their nestlings (usually insects in most polygynous species) wi thout male assistance. In the lek-mat ing ty rann id flycatcher Pipramorpha oleaginea, for example , male emancipation results f rom a f rugivorous diet, a p e n d a n t nest tha t is safe from p reda to r s , a n d female regurgi ta t ion of food to the chicks, which is an unusua l behavior in flycatchers (Snow a n d Snow, 1979).

Frugivory is necessary bu t no t sufficient to p r o m o t e the evolution of lek mat ing in bi rds of paradise (BOPs). Beehler a n d Pruet t -Jones (1983) indicate tha t polygyny a n d nonter r i tor ia l spacing systems only occur in BOPs whose diets include over 50% fruit; insectivorous species a re m o n o g a m o u s a n d terr i torial . F u r t h e r m o r e , a m o n g the frugivores, only species feeding on the nut r i t ious arils of capsular fruit of the Meliaceae or Myristicaceae a re polygynous. Fig-eating m a n u c o d e s a re m o n o g a m o u s , a n d both pa ren t s feed these nutr i t ionally p o o r fruit to their nestlings.

Beehler (1989) identifies t h r ee factors that p r o m o t e the evolution of polygyny a n d lek ma t ing in bi rds of paradise . T h e s e include:

1. a c l u m p e d dis t r ibut ion of fruits which allows displaying males to be exposed to many females with over lapp ing h o m e ranges ;

2. h igh s p a t i o - t e m p o r a l predictability a n d high nu t r i en t con ten t of capsular fruits a n d insects, which allows females to feed their nestlings wi thout male assistance; a n d

3. large female h o m e ranges , which are n e e d e d to harvest capsular fruits p r o d u c e d in low daily n u m b e r s over ex t ended per iods of t ime.

Large over lapp ing female ranges allow certain males to set u p strategically placed display sites, which at tract o the r males as well as females. Dispersion of males within a lek will d e p e n d , in par t , on the skew in male mat ing success. A s t rong skew with one male accruing most of the copulat ions at a lek will favor large, tightly c lumped leks (as in Raggiana BOPs) whereas m o r e equal ma t ing success a m o n g males will p r o m o t e exploded leks (as in magnificent BOPs) (Beehler a n d Foster, 1988). Preda t ion may also be involved because t ight leks occur in species living in second growth or a long forest edges w h e r e r a p t o r densities a re high (Beehler a n d Pruet t -Jones , 1983).

Like BOPs, most f rugivorous bowerbi rds a re t h o u g h t to be polygynous, a l though this has been conf i rmed in only a few species (Diamond, 1986). In contrast to manucodes , fig-eating catbirds (Ailuroedus) a re terr i torial a n d m o n o g a m o u s . In most o the r species, males a re nonter r i tor ia l except in the


immedia te vicinity of thei r bowers , which t end to be evenly spaced to minimize the stealing of bower materials a n d d is rupt ion of ma t ing displays. Only females bui ld nests a n d care for nestlings.

It should be no ted that no t all f rugivorous birds ea t ing nut r i t ious capsular fruits a re polygynous, a n d not all lek-mating frugivorous birds eat capsular fruits. For example , n o n e of the major consumers of neot ropical Virola fruits (Myristicaceae), inc luding toucans , a guan , a motmot , a n d the masked tityra, a re polygynous , n o r is the r e sp l enden t quetzal , a specialist on nu t r i t ious fruits of the Lauraceae (Howe, 1987; Wheelwright , 1983). Likewise, the diets of lek-mat ing manak ins , small b i rds of neotropical forest unde r s to -ries, include mostly berr ies or small d r u p e s (Wor th ington , 1982), a n d polygynous neotropical cotingids (e.g., cock of the rock) d o no t specialize on capsular fruits (Snow, 1976). T h u s , while frugivory permits lek-mating in certain g roups of tropical bi rds , diets of lek-maters have not converged on a na r row subset of highly nut r i t ious fruits with a par t icular set of phenological characteristics. As a result , a single resource scenario canno t be devised to explain the evolut ion of lek ma t ing in frugivorous birds.

With the possible except ion of the insec t ivore- f rugivore Mysticina tubercu-lata (Mystacinidae) of New Zealand (M. Daniel a n d E. Pierson, personal communica t ion , 1991), lek ma t ing occurs only in f rugivorous bats of the e p o m o p h o r i n e (or epauletted) g r o u p of African p te ropod ids . In species of Epomops, Epomophorous, Hypsignathus, a n d Micropteropus, males spend several h o u r s each n igh t d u r i n g the ma t ing season calling f rom tradi t ional sites before r a n g i n g widely in search of fruit (Bradbury , 1977; T h o m a s a n d Marshall , 1984; Wickler a n d Seibt, 1976). Leks a re not located nea r concentrat ions of fruit, a n d lekking species eat the fruit of bo th p r imary a n d secondary forest plants (e.g., of the gene ra Ficus, Solarium, Musanga, a n d Anthocleista). Lek ma t ing is u n k n o w n in f rugivorous phyl lostomid bats. Instead, polygynous ma t ing based on roost site or female defense is the ru le in these bats, as well as in many species of f rugivorous p t e r o p o d i d bats (Fleming, 1988).

T h e ma t ing systems of f rugivorous pr imates include m o n o g a m y a n d polygamy ( including po lyandry a n d polygyny). Resource-patch size a n d p reda t ion risk a re i m p o r t a n t c o m p o n e n t s of models of opt imal g r o u p size a n d ma t ing systems in pr imates ( T e r b o r g h , 1983; W r a n g h a m , 1987). For example , bo th T e r b o r g h a n d W r a n g h a m postulate that resource-pa tch size de t e rmines opt imal g r o u p size for females, a n d that male dis tr ibut ions reflect female dis t r ibut ions. Accord ing to T e r b o r g h , large food patches pe rmi t the format ion of g r o u p s of females a n d accompanying males, a n d opt imal g r o u p size is d e t e r m i n e d by a t radeoff between compet i t ion for food a n d protec t ion f rom p reda to r s .

S u p p o r t for the impor t ance of food-patch size in d e t e r m i n i n g g r o u p size comes f rom a compar i son of the social systems of sympatr ic congener ic pr imates (e.g., leaf monkeys , macaques , colobus, and lemurs) , in which one


species lives in small g roups with a single adul t male and the o the r lives in larger g roups with several adul t males ( T e r b o r g h a n d J a n s o n , 1986). In each case, the species living in the small g r o u p is m o r e folivorous a n d has a smaller daily r a n g e t han the o the r m o r e frugivorous species. T h e s e au thors suggest that single male g roups occur in 4 3 % of all folivorous p r imate species c o m p a r e d with only 15% of f rugivorous pr imates , because folivores have m o r e t ime to de fend a n d monopol ize females than d o frugivores. S u p p o r t for the impor t ance of p reda t ion as a critical factor comes f rom the fact that m o n o g a m o u s species t end to be e i ther relatively small a n d noctur nal (e.g., Aotus), o r large (i.e., > 1 0 kg) and d iu rna l (e.g., Hylobates, Sym-phalangus) ( T e r b o r g h a n d J a n s o n , 1986). Small g roups a re favored in noctu rna l species to r educe their detect ion by auditori ly or ien t ing p reda to r s , whereas large species a re too big for most p reda to r s to kill.

b. Patterns in Nectarivores Polygynous mat ing systems a re the rule in h u m m i n g b i r d s , whereas m o n o g a m y rules in passer ine nectar ivorous families (Collins a n d Paton, 1989). "Clearly the [food] exploitat ion systems of h u m m i n g b i r d s a re intimately related to their social systems; the two a re tightly in tegra ted in the ecology of any h u m m i n g b i r d species" (Stiles a n d Wolf, 1979, p . 71). T w o social systems p r e d o m i n a t e in h u m m i n g b i r d s — food-centered terr i tor ies a n d lek mat ing systems. In the fo rmer system, males of socially d o m i n a n t species de fend highly c lumped patches of flowers against conspecific males a n d o the r species, and females a re allowed into terr i tor ies to mate . In the lat ter system, males congrega te in g roups away from concen t ra ted resources a n d attract females with calls. In bo th systems, females build nests a n d care for their two-egg clutches alone. Food-based terr i tor ies a re found in m o r e species t han a re leks, which occur only in socially subord ina te he rmi t h u m m i n g b i r d s . T h e absence of polygynous mat ing systems in o the r kinds of nectar ivorous birds indicates that nectarivory may be necessary bu t not sufficient for the evolution of polygyny.

T h e b r e e d i n g systems of nectar ivorous bats a re poorly known. Most species probably a re polygynous, bu t n o n e is known to be lek mat ing . Nectar ivorous m e m b e r s of the Phyllostomidae, whose roost ing behavior is known, a re gregar ious roosters , a l though it is likely that sexual segregat ion occurs in some species d u r i n g par tur i t ion times (Fleming, 1988). Roost sizes in these species r a n g e f rom dozens to a few h u n d r e d individuals in Glosso-phaga soricina, to t housands of individuals in Leptonycteris curasoae. Most flower-visiting m e m b e r s of the P te ropod idae a re also gregar ious roosters , somet imes living in large colonies (e.g., Eonycteris spelea). Austra l ian blossom bats (Syconycteris), in contrast , a re solitary roosters (Richards, 1983b). Except in solitary roosters , ma t ing systems in nectar ivorous bats probably involve e i ther female o r roost site defense, as is the case in f rugivorous bats.


IV. Conclusions

In this c h a p t e r I have addressed the hypothesis that various c o m p o n e n t s of the life histories of fruit- a n d nectar-eat ing birds a n d m a m m a l s have been significantly inf luenced by the s p a t i o - t e m p o r a l variability of the i r food resources . I have d e m o n s t r a t e d that densities of fruits a n d flowers can be highly variable in space a n d t ime a n d that these resources probably w a r r a n t be ing called patchy. I recognize, however , that this designat ion needs to be m a d e m o r e opera t iona l a n d that fruit a n d flower densities need to be m o r e tho rough ly quantif ied, especially with respect to the daily a n d seasonal energet ic needs of frugivores a n d nectar ivores. Careful resource moni tor ing should be a top priori ty in any ecobehavioral s tudy of these animals .

My review of the d e m o g r a p h y , movement s , a n d social organizat ion of frugivores a n d nectar ivores provides s t rong circumstantial evidence tha t resource variability has i ndeed h a d a s t rong influence on the evolut ion of their life histories. T i m i n g of b reed ing , overall a b u n d a n c e , popula t ion fluctuat ions, daily a n d seasonal m o v e m e n t pa t te rns , intra- a n d interspecific social interact ions, a n d ma t ing pa t t e rns a p p e a r to be sensitive to resource condi t ions in at least some g roups of fruit- or nectar-eat ing birds a n d m a m m a l s . But statistical correlat ions d o not necessarily allow us to reach s t rong conclusions r e g a r d i n g cause-and-effect relat ionships beh ind these correlat ions. S t rong inferences abou t unde r ly ing causes a n d effects in biology usually r equ i r e an exper imen ta l a p p r o a c h — a n a p p r o a c h that is virtually impossible to p u r s u e w h e n deal ing with highly mobile species of birds a n d m a m m a l s .

A compara t ive a p p r o a c h in which phylogenet ic effects a re carefully controlled (e.g., Harvey a n d Read, 1988) would seem to be the nex t best m e t h o d for m o r e critically u n d e r s t a n d i n g the relat ionships between resource variability a n d the evolut ion of life histories. T h r o u g h o u t this chap te r , I have informally used a compara t ive a p p r o a c h by men t ion ing how frugivore a n d nectar ivore life histories differ f rom those of o the r diet classes. F r o m an evolut ionary perspect ive, the best compar i son in bi rds a n d phyllostomid bats (and probably also in pr imates) , is be tween insectivores a n d frugivores o r nectar ivores , because the lat ter two g roups a p p e a r to be der ived f rom insectivorous ancestors , a n d / o r still have relatives that a r e insectivorous (Feduccia, 1980; Hill a n d Smith, 1984). I n d e e d , many species of nectarivorous o r f rugivorous birds , bats, a n d pr imates still occasionally feed heavily on insects.

Results of this informal compar i son indicate that , relative to insectivores, frugivores a n d nectar ivores a re m o r e likely to

1. have seasonally variable popula t ion sizes and communi ty composi t ions, 2. u n d e r g o seasonal habi ta t and elevation shifts, 3. be nomadic ,


My research on f rugivorous a n d nectar ivorous bats has been generously s u p p o r t e d by the U. S. Nat ional Science Founda t ion , Nat ional Geographic Society, Nat ional Fish a n d Wildlife Founda t ion , and by a Fulbr ight Fellowship. I t h a n k J . Kar r a n d B. Loiselle for p rovid ing m e with p r ep r in t copies of some of thei r pape r s . I also t hank J . Kar r for critically r ead ing a draft of this pape r . Th i s is Cont r ibu t ion No . 368 from the P r o g r a m in Ecology, Behavior, a n d Trop ica l Biology, D e p a r t m e n t of Biology, University of Miami.

Acknowledgments

Appendix

Scientific names of the b i rd species men t ioned in the text.

Amer ican robin Cock of the rock Buff-tailed sicklebill

Turdus migratorius Rupicola rupicola Epimachus albertisi

Gray catbird Magnificent b i rd of parad ise

Dumatella carolinensis Diphyllodes magnificus

Masked tityra Mistle t h r u s h

Tityra semifasciata Turdus viscivorous

4. travel in intraspecific flocks (frugivores and Austral ian honeyeaters) , and 5. have lek mat ing systems or be polygynous (birds). 6. be terr i torial (frugivores only).

While a statistical analysis based on multivariable quanti tat ive da ta would certainly be desirable as a m o r e r igorous compara t ive test of my major hypothesis , I believe tha t da ta in h a n d provide m o r e than simply circumstantial s u p p o r t for this hypothesis . I the re fore conclude that the life histories of frugivores a n d nectar ivores have been strongly affected by the s p a t i o - t e m p o r a l variability of their food resources .

As m e n t i o n e d in the in t roduct ion , fruit- a n d nectar-eat ing birds and m a m m a l s play i m p o r t a n t roles as seed dispersers a n d poll inators in many communi t i es . Because of their daily a n d seasonal movements , these species clearly serve as mobile links be tween plant popula t ions and communi t ies over large geograph ic areas (e.g., Fig. 4). T h e des t ruct ion of habitats and their resources a long al t i tudinal o r lat i tudinal fruit a n d nectar pathways clearly will affect the lives no t only of the migrants , bu t also of their food populations e lsewhere in thei r annua l cycle. Conservat ion of habitats within these pathways is vitally impor t an t . Otherwise , species as mobile as frugivores and nectar ivores a re d o o m e d to extinction.


New Hol land honeyea te r Raggiana b i rd of pa rad i se Resp lenden t quetzal Scarlet honeyea t e r T r e e swallow T r u m p e t m a n u c o d e White-eyed vireo Whi t e -naped honeyea te r Yellow-faced honeyea te r

Phylidonyris novaehollandiae Paradisaea raggiana Pharomachrus mocinno Myzomela sanguinolenta Iridoprocne bicolor Manucodia keraudrenii Vireo griseus Melithreptus lunatus Lichenostomus chrysops

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