Ecology, 66(3), 1985, pp. 808-818@ 1985 by the Ecological Soctety of America

FRUIT SIZE, GAPE WIDTH, AND THE DIETS OFFRUIT -EATING BIRDS!

NATHANIEL T. WHEELWRIGHT2Department oj.Zoology, University of Florida, Gainesville. Florida 326Il USA

,.

Abstract. In most animals, especially those that must swallow food items whole, prey size isrelated directly to predator size. This paper examines gape limitation and the influence of fruit sizeon diet in fruit-eating birds, drawing on data gathered over a 5-yr period on 70 bird s]Jecies and 171plant species in the lower montane forests of Monteverde, Costa Rica. The results suggest that fruit-eating birds face many of the constraints imposed on other gape-limited foragers, but ruive an unusualminimum-size relationship with their food because of the unique characteristics of fruilts. Fruit-eatingbirds with broad gapes consumed more lauraceous fruit species and a larger mean and IlDaximum sizeof fruits overall than narrow-gaped birds. However, the size of the smallest fruits eaten was notcorrelated with gape width; large-gaped species commonly fed on diminutive fruits. Birds effectivelyselected among individual fruits within a tree on the basis of fruit size, dropping bulky fruits beneaththe tree. Effective size selectivity also occurred among trees of different species in the same familyand among plant species in various families. The diet of broad-gaped birds was not c;omprised dif-ferentially of large fruit species. For example, Three-wattled Bellbirds favored mediUlID-sized fruits,whereas Long-tailed Manakins took individual fruits in the same proportions as they to()k fruit speciesof different mean fruit diameters. Gape limitations and effective size selectivity have obvious con-sequences for seed dispersal patterns: plants with large fruits attracted fewer species of birds thanplants with small fruits. Moreover, the broad-gaped bird species on which large-fruited plants spe-cialized were those with the most generalized diets.

Key words: body size; Costa Rica; frugivory; fruit-eating birds; fruit size; gape-limited predators;gape width; seed dispersal; size selectivity; tropical forests.

INTRODUCTION

Most fruit-eating birds feed on only a portion of thediversity of fleshy fruits produced in any habitat (Snow1970, Snow 1981). Fruit selection presumably dependson the behavior, morphology, and nutritional require-ments of birds, the abundance of alternative food re-sources, and fruit characteristics such as temporalavailability, habitat, taste, color, abundance, andplacement on a plant (Thompson and Willson 1978,1979, Denslow and Moermond 1982, Howe 1982,Morden-Moore and Willson 1982, Sorensen 1983,Wheelwright and Janson 1985). Fruit characterisics suchas pulp-to-seed ratio and nutrient composition alsopartly determine the net value of a fruit (Howe andVande Kerckhove 1980).

Fruit size may be critical to selection, but it has beengiven surprisingly little consideration, despite the dem-onstration in many foraging studies that the sizes ofpredators and prey are often positively correlated (Hes-penheide 1973, Wilson 1975). Small-fruited plantspecies have been hypothesized to attract more speciesof birds than large-fruited ones (Terborgh and Dia-mond 1970), although Kantak (1979) found that in-termediate-sized fruits drew the largest number of birdspecies among the five plant species she studied inMexico. Bill size in Panamanian flycatchers and tan-agers appeared to be correlated with the size of pre-

ferred fruits (Leck 1971). Diamond (1973) reportedthat New Guinea fruit pigeons :lgnored fruits that weresmall relative to their own size; big birds ate big fruits,medium birds ate medium fullits, and so on. Snow(1973) noted the correspondence between bellbird(Procnias spp.) gape widths and the sizes of their fa-vored fruits, species in the Lauraceae, and recognizedthat fruits, if too large, would not attract seed dispers-ers.

This paper explores the pattc~ms, mechanisms, andconsequences of effective fruit size selectivity by birdsin a species-rich tropical forest. In particular, it ex-amines whether gape size conslcrains a bird's diet andwhether large fruit size restric-ts the number of birdspecies that can serve as potential seed dispersers fora plant species. Most fruit-eatulg birds are "gape-lim-ited" (Zaret 1980). They typicalJly swallow fruits whole,although a few soft fruits such as Ficus spp. may beeaten piecemeal. Even tanagc:rs, which commonlymandibulate fruits to remove sec:ds, cannot handle largefruits (D. Levey, personal communication; N. Wheel-wright, personal observation).

The following predictions we~re tested. As in manygape-limited predators (Zaret 1980), (1) size of the larg-est fruit eaten by birds should be closely correlatedwith gape width, (2) large birds should eat more fruitspecies and a wider range of fnlit sizes, and (3) meansize of fruits included in the dit:t should be positivelycorrelated with gape width. However, in contrast tothe case of many carnivores (Rosenzweig 1966; see alsoDiamond 1973), (4) gape width and size of the smallestfruit eaten should not be correlated; even minute fruits

I Manuscript received 25 July 1983; revised 24 May 1984;

accepted 1 June 1984.2 Present address: Section of Ecology and Systematics, Cor-

nell University, Ithaca, New York 14853 USA.

June 1985 FRtJIT SIZE AND BIRD GAPE WIDTH 809

TABLE 1. Fruit diameters, observation times, number of censuses, and bird species recorded at 1~; tree species, each observedfor at least 4 h at Monteverde, Costa Rica.

Number of bird species observed during

2.22.31.71.21.81.91.81.21.72.21.21.31.20.80.6

26.55.8

14.06.8

18.526.06.0

37.817.07.04.64.0

23.16.07.0

204316344204848876

4984848316120428316695

323341044

323343084236657

4578554

1854589

1413

6556

~ -

.13 species in the Lauraccae plus Hasse/tia (Flacourticcae) and Oreopanax (Araliaccae).

tend to be conspicuous and easy to capture, unlikeminute animal prey. Finally, (5) plants producing smallfroits should attract more species of birds than large-fruited plants. Three types of data were used to testthese predictions: the sizes of seeds regurgitated bybirds versus the sizes of seeds from fruits dropped un-eaten by birds; the number of froit species of a singleplant family (Lauraceae) eaten by birds; and the num-ber and sizes of froit species of all plant families eatenby birds.

STUDY SITE AND METHODS

Study area

For 21 mo between June 1979 and February 1984,I studied fi"uit-eating birds and fruiting patterns in bird-dispersed plants in the lower montane wet and rainforests of Monteverde, Costa Rica (10°18' N, 84°48'W; Holdridge 1967). The study area (elevation 1350-1550 m) of ~ 15 km2 includes several habitat typesmaintained by a moisture gradient due to the prevailingnortheast trade winds passing over the continental di-vide (see Lawton and Dryer 1980 for a more completedescription of the site). Portions of the undisturbed2700-ha Monteverde Ooud Forest Preserve, as well asscattered pastures and woodlots, made up the studyarea.

Determining bird diets

No single sampling technique could be used to de-termine the diets of such an ecologically diverse groupof fruit-eating birds as occurs at Monteverde. There-fore, I combined various techniques to learn what fruitsbirds ate. The most thoroughly sampled diets werethose of birds that use fixed perches, below which Iplaced "seed traps" (Snow 1970, Wheelwright 1983).

Seeds from> 2500 fruits were recovered beneath call-ing perches of Three-wattled Bellbirds (Procnias tri-caruncuJata), nest-guarding perches of ResplendentQuetzals (Pharomachrus m.?cinno), and courtshipbranches of Long-tailed Manakins (Chiroxiphia lin-earis). I spent> 300 h watching birds feeding at variousfruiting trees (including species listed in Table I; cf.Howe 1977). During the fruiting seasons of 15 speciesin the Lauraceae, I made weekly 1-4 h morning ob-servations offoraging birds at <iifferent individual treesof each species (median = 7.0 h/species). I also con-

ducted separate biweekly censuses of birds at a medianof 10 trees per species (WheerNright 1985; species arelisted in Table 1). For each of 28 species in other plantfamilies, I spent 2-8h/species "watching at one or moreindividual trees during the peak of fruiting, and! or made> 20 censuses of various trees ,on different days duringthe same period. These species, plus the 15 lauraceousspecies described above, are here referred to as me-thodically studied, as opposed to 88 other plant speciesstudied less extensively; for :m additional 37 plantspecies I made only occasional observations. Becausethis study spanned nearly 5 yr during which variousaspects of individual tree species were examined, ob-servation times, census numbers, and sample sizes oftendiffered among plant species. I made additional ob-servations by following flocks for> 2000 h in the field.Censuses and miscellaneous observations proved to bemore important than watches at trees for recordinguncommon or furtive bird species (Table I; cf. Howe1977). Various biologists sharelj additional feeding ob-servations (K. G. Murray, C. Ciuindon, and R. LaVal,personal communication).

Despite the fact that the feeding habits of fruit-eatingbirds at Monteverde are as well known as those of any

810 NATHANIEL T.

other tropical forest,judging from Snow's (1981) globalsurvey of avian frugivory, the data analyzed here aredoubtless incomplete. Much of the original data arepresented in Wheelwright et al. (1984), where samplingbiases are discussed in detail. Although observationconditions, habitats, and amount of time spent watch-ing at plants were not identical for each species, therewere no known systematic biases with regard to fruitsize or other traits (except for the Lauraceae; see below),nor were there significant differences in fruit dimen-sions between groups studied methodically or only cas-ually (Mann-Whitney U test: P> .05, n = 43 and 88

species, respectively).Fruits rarely require crushing (in contrast to seeds;

Willson 1971) or dexterous manipulation (in contrastto fish; Ashmole 1968), but a major problem fruit-eating birds face in eating their food is simply swal-lowing it. Gape width was, therefore, assumed to de-termine the upper size limit of food items that can beeaten whole. Esophagus diameter, interclavicular dis-tance, and gizzard volume could also be importantlimiting factors, but they are difficult or impossible tomeasure on museum specimens. Gape width, the ex-ternal distance between commissural points, was mea-sured to within 0.1 mm with calipers on museum spec-imens of 89 species of fruit-eating birds found atMonteverde (70 of which were observed eating fruitsin this study; see Wheelwright et al. 1984). Sample sizesranged from two (male and female) to nine individualsper species; mean gape width was calculated for eachspecies. Measurements of gape width were 5% narrow-er for museum specimens of Emerald Toucanets (Au-lacorhynchus prasinus) than for live birds (n = 3 and4, respectively), but were similar for prepared and livequetzals (n = 4 and 1, respectively). Gape width wascorrelated with bill depth and length in nine Monte-verde fruit-eating bird species for which I have com-plete morphological measurements (Spearman rankcorrelation, width vs. length: r, = 0.80; width vs. depth:r, = 0.78, P < .01) (see also Willson 1971).

Sampling procedures and fruit measurements

In determining the size distribution of available "birdfruits," I included all plant species whose fruits birdswere seen eating as well as all fruits that had charac-teristics clearly corresponding to van der Pijl's (1969)syndrome of bird fruits: odorless, fleshy fruits, usuallypersistent on the plant and often brightly colored (seeJanson 1983). Fresh fruits were measured to within 0.1mm with calipers. In this study I focused on fruit di-ameter as the dimension most likely to be restrictivein "gape-limited" birds, reasoning that relatively longfruits (e.g., Tetragastris; Howe 1982) can be swallowedby many bird species if the fruits are not too broad(but see description of Beilschmiedia costaricensis be-low). Pericarp and seeds were weighed to within 0.01g with a spring balance. Fruits of the Lauraceae weresampled haphazardly from 2 to 25 individual trees per

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RESUL n;

Fruit sizes and g,zpe widths

Fruits observed to be eaten b~{ birds and those merelypresumed to be (e.g., corresponding to van der Pijl's[1969] syndrome of avian seed dispersal) did not differsignificantly in fruit diameter (Mann-Whitney U test:P = .39, n = 131 and 115 species, respectively), length

(P=.26,n= 131andl15),ormass(P=.09,n= 114and 100), even when the large-fruited Lauraceae wereincluded. Therefore, in the de:scriptive analyses pre-sented in this section, these sa.mples were combined.Fruits ranged in diameter frol1rl 2 to 28 mm (Fig. 1).The majority of plant species 1~69.1%) had fruits with

WHEEL WRIGHT Ecology, Vol. 66, No.3

species. I used a slingshot to propel lead weights at-tached to monofilament linc~ over 10-30 m highbranches. Pulling on the line, [ could shake ripe fruitsoff or break brittle fruit-bearing branches. In two speciestested (Phoebe mexicana and Ocotea bernou/iana), fruitand seed dimensions were independent of position inthe tree (Mann-Whitney U test: P> .05). Over 2800fruits and seeds were measufl:d (median = 47 fruits

per species).For most species outside of the Lauraceae, 3-5 rep-

resentative fruits were selected Jrom one or more plants.Fruits were collected throughout the study by followingfruit-eating birds or searching at regular intervals alongestablished transects. In total «:ounting the Lauraceae),fruits of 246 plant species were: measured. To estimatethe maximum likely deviation between sample andpopulation means, I measured an average of 51.1 fruitsfrom 2-25 individual plants oj: each of 15 species. Foreach species, three fruits were l:andomly selected usingrandom number tables, and ml~an values oftotai mass,net pulp mass, and the ratio of seed mass to fruit masswere compared to values derived from the larger sam-ples from which they were drawn. Average deviationsfor the three variables from small vs. large sampleswere 8.4%, 8.6%, and 4.7%, respectively. Measure-ments of even small samples, therefore, gave a reason-able indication of a species' rank relative to otherspecies. Moreover, sample means for the 246 plantspecies probably deviated far l(:ss from true populationmeans than did the random e~mples presented above,because I deliberately chose typical fruits (based onknowledge of the range of variability within the pop-ulation and individual plants).. In any event, it is un-likely that the sampling procedure biased the resultsin any systematic way, because the same procedurewas used for fruits of all sizes. This study did not in-clude for consideration birds t1:lat eat fruits but destroymost seeds (e.g., parrots) or fnuts whose seeds appearto be dispersed mainly by wind, insects, or mammals.Sample sizes vary in differen1: analyses where infor-mation was incomplete for cel1ain species. All statis-tics, except where noted, are nonparametric (Siegel1956).

June 1985 FRUIT SIZE AND BIRD GAPE WIDTH 811

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246 PlANTSPP.

/89 FRUIT-EATINGBIRD SPP.~

0..(J)

u.0

0'z

'-,3010 15 20 25 --

FRUIT DIAMETER OR GAPE WIDTH (mm)

FIG. 1. Frequency disuibutions of mean diameters offruitsof diffCl~nt species eaten (or presumed eaten; see Methods:Sampling Procedures and Fruit Measurements) by birds (-and 8; n = 246 species) at Monteverde, Costa Rica, and gapewidths of co-occurring fruit-eating birds (--- and 0; n =89 species). Medians of distributions indicated by arrows abovehorizontal axis.

a mean diameter of 5-12 mm; the distribution of fruitdiameters showed a second peak near 17 mm. Meanand median fruit diameters were 10.1 mm and 9.0 mm,respectively (n = 246 plant species). Mean and medianfruit masses were 1.16 g and 0.46 g, respectively (n =

214). Fruit diameter was highly correlated with fruitlength (n = 246 species, Spearman rank correlation:r, = 0.88, P < .001) and mass (n = 214 species, r, =

0.92, P < .001). About half (48.9%) of the species had

single-seeded fruits; only 23.8% had more than 10 seedsper fruit. The median ratio of seed mass to fruit masswas 0.21 (n = 214 species). Single-seeded fruits were

significantly larger and had greater seed mass to fruitmass ratios than multi-seeded fruits (Mann-WhitneyUtest: P < .001) (see Wheelwright et al. 1984).

The distribution of gape widths offruit-eating birdsat Monteverde paralleled that of fruit diameters (Fig.I). The median gape width of 89 bird species was 11mm, and most bird species had gapes measuring 8-13mm across. Gape width and fruit diameter distribu-tions were significantly different (Kolmogorov-Smir-nov two-sample test: P < .01), but their shapes were

similar and they did not differ in dispersion or skewness(P > .05).

Observations within plant species

To test the hypothesis ofetfective fruit size selectivityby birds, I compared the sizes of seeds regurgitated bybirds with seeds from fruits dropped by birds or col-lected randomly from trees of two species ofLauraceae.

Beilschmiedia costaricensis bears bulky black fruitsranging from 17.4 to 25.2 mm in diameter within asingle tree. Ripe fruits, irrespective of size, remainedon the tree for many months until plucked by an an-imal. Seed diameter measured 11.7 to 26.7 mm within

11 12 13 14 15 16 1"7 18 19 20

SEED DIAMETER (mm)

FIG. 2. Frequency distributions of diameters of Beil-schmiedia costaricensis (Lauraceae) seeds regurgitated belowan isolated tree by Emerald Toucanets (Aulacorhynchus pra-sinus) (&I; n ~ 43), YS. seed diameters of fruits dropped un-eaten by birds below the same tree (0; n = 37).

the population, and was highly correlated with fruitdiameter(r, =0.92, n = 89, P < .001). Seed length wascorrelated with both fruit leni~th (r, = 0.95, P < .001)and seed diameter (r, = 0.80, P < .001). B. costari-censis fruits were far too massive (X = 12.9 g) for mostbirds to handle, but five of the largest bird species,including Emerald Toucanets.. fed commonly on them(Wheelwright et al. 1984). Unlike quetzals and bell-birds, toucanets did not habitually return to a specificperch where regurgitated seed:s could be sampled usingseed traps, so I collected all seeds that I could findregurgitated by a toucanet flock foraging alone at anisolated pasture tree between 3 and 14 January 1981.The diameters of seeds regurgitated (and, by inference,fruits consumed) were smalle:r than the diameters ofseeds from fruits dropped by the birds beneath the tree(Mann-Whitney two-sample 1:est: n = 43 regurgitatedseeds and 37 seeds from fruits, most with bill marks,recovered in a complete sample below the tree; P <.00 I; see Fig. 2). The concl\Jlsion that toucanets atesmaller fruits than expected is based on the assump-tions that, after being swallo",ed, seeds were not de-posited differentially according to size and that the sizesof fruits eaten were correlated with the sizes of seedsregurgitated. Similar results with quetzals and bellbirds(see below) support such assumptions. (At least tworeasonable but untested hypotheses argue for differ-ential dispersal according to sc-'ed size, with contradic-tory predictions: [I] large fruits take longer to digestthan small fruits [N. Wheelwright, personal observa-tion], and therefore their correspondingly large seedsmay be carried farther from fruiting trees; [2] birdsmay tend to remain close to fruiting trees after ingestinglarge fruits because the seeds of large fruits are espe-cially bulky.)

Seeds of the same species recovered from seed trapsbeneath quetzal and bellbird I;lerches also reflected anupper size limit to fruits swallowed. The largest regur-

812 NATHANIEL T. WHEELWRIGHT Ecology, Vol. 66, No.3

10 15 20 25 30

GAPE WIDTH (mm)

FIG. 3. Gape widths of bird:~ Ys. number of species oflauraceous fruits eaten (r. = 0.6~~, n = 17 bird species, P <0.01; equation of the linear regression: Y = 0.6X -4.8).

gitated seeds did not exceed 20 mm in diameter forbellbirds or 23 mm for quetzals, as compared to amaximum seed diameter of > 26 mm among randomlyselected fruits (n = 35 seeds selected, using a random

number table, from a larger exhaustive sample offruitsdropped by birds below 10 different B. costaricensistrees). Seeds regurgitated by bQth quetzals and bellbirdswere significantly shorter than seeds from the samesample of dropped fruits (quetzals: n = 52 regurgitatedseeds; bellbirds: n = 19 regurgitated seeds; P < .001),

although they were not significantly smaller in diameter(P > .05). Quetzals and bellbirds did not differ in thediameters or lengths of B. costaricensis seeds regurgi-tated (P > .05). A sample size of 52 B. costaricensisseeds is equivalent to a large bird's total fruit con-sumption over a 3-5 d period. (The fruits take 40-70min to digest [N. Wheelwright, personal observation)and even the larger birds [with the exception of BlackGuans, Chamaepetes unicolor) can process only onefruit at a time; during a 12-h foraging day, a bird canconsume only 10-18 fruits.)

The diameter of Ocotea tonduzii fruits (9.7-13.2 rom)was also correlated with seed diameter (4.2-10.4 rom;rs = 0.80, n = 199, P < .001). Moderate-sized fruits

probably pose few handling problems for larger birdsbut may be too big for small birds such as manakins(gape width 8.5 mm). Ocotea tonduzii fruits repre-sented < 1 % of all fruits eaten by manakins (n = 844),so few seeds were recovered from traps suspended be-neath male manakin courtship perches. Nonetheless,regurgitated seeds were significantly smaller in diam-eter than seeds from randomly selected fruits (Mann-Whitney U two-sample test: n = 8 regurgitated seedsand 38 seeds selected, using a random number table,from a larger sample of fruits taken from 10 differento. tonduzii trees; P < .001). o. tonduzii seeds regur-gitated by bellbirds (n = 22) were not significantly dif-ferent in size from the random sample (P = .08). Seedscollected in traps beneath two quetzal perches (n = 44)were significantly larger than the random sample (P <.01), and seeds regurgitated by both bellbirds and quet-zals were larger than seeds regurgitated by manakins(P < .001). Some effective size selectivity probably oc-curs simply because birds' nests or perches happen tobe located near a large- or small-fruited tree. O. ton-duzii seeds recovered beneath bellbird (n = 22) andquetzal (n = 22) perches located only 100 m apart weresignificantly different in size, and both samples weresmaller than those regurgitated by a second quetzal pair(n = 22) several hundred metres away (Mann-WhitneyU test: P < .01).

:1;J,:J~

mm to 24.8 mm in 23 bird-dispersed species (Wheel-wright et al. 1984). By studying a single plant familyin detail, I tried to isolate the effects of fruit size whilecontrolling for confounding visual or nutritional traits.

The number of species of uluraceous fruits eaten bya bird species was positively correlated with its gapewidth (Fig. 3; r. = 0.64, n = 17 bird species, P < .01).

Toucanets ate fruits of at leas"t 19 of the 23lauraceousspecies. Manakins were obsc~rved feeding at only 1speci~s, whereas Mountain It-obins fed on 9 species(Wheelwright et al. 1984). Tile fact that there was nocorrelation between gape size, and frequency of visitsto lauraceous trees by 17 bird species (Spearman rankcorrelation; P > .05) indicate5: that these results are notsimply due to the increased conspicuousness or abun-dance of large-gaped birds, which, in fact, have lowerpopulation sizes than most small-gaped fruit-eatingbirds at Monteverde. Many common species of fruit-eating birds, e.g., manakins, Black-faced Solitaires(Myadestes melanops), Olive-striped Flycatchers(Mionectes olivaceus), appear l:arely if at all at the large-fruited lauraceous trees. DuriJ!1g > 200 h of systematictree-watches at all lauraceous species, Mountain Rob-ins accounted for 46.1% of 2.337 visits by birds, tou-canets 26.4%, quetzals 11.5'%, bellbirds 3.6%, andWhite-throated Robins (Turcius assimilis) 2.3%. Noother bird species represented> 1 % of 0 bserved visits.

Observations among all plant species

The number of fruit species of all plant families in-cluded in the diets of32 well-studied bird species (eachwith at least five different fruilt species recorded eaten[five "fruit records"]), was not significantly correlatedwith gape width (r. = 0.32, P = .09), due in part to thelarge numbers of fruit specie5, eaten by several small-gaped species, including manakins and Black-facedSolitaires. Large birds tended to eat a broader size range

Observations within a plant family

Another test of the hypothesis that fruit size and gapelimitations affect diet is to examine fruit choice by birdsamong plant species in the same family. Fruit traitssuch as color and nutrient composition varied littlewithin the Lauraceae, but diameters ranged ftom 8.0

June 1985 FRUIT SIZE AND BIRD GAPE WIDTH 813

A25

EE

~20

~WI-~ 15<isI- 10:5~u.

5

........." ..§ ..0

8MAXIMUM

@MINIMUM

0

0 80 oa,os,O 0 00 0 0

0 0 0 0 0

.

301

B25

EE

-20

~WI-W 15~<0I- 105~u.

t+.

00 5 10 15 20 is 3"0 35

GAPE WIDTH (mm)

FIG. 4. (A) Maximum and minimum diameters and (B)mean diameter (:t I SD) of fruit species included in the dietsof 32 well-studied bird species. In this figure and in Figs. 5-6, it appears that some birds fed on fruits larger than theirgapes. Such feeding records are probably due to the fact thatbirds may feed selectively on small fruits within a plant (i.e.,fruits smaller in diameter than the mean values used in thesefigures). Also, birds can swallow fruits that are slightly widerthan their gape because the rami of the mandibles are flexible.

large birds such as toucanets and guans were not dis-proportionately composed of large fruit species (Fig.5a-d, Fig. 6; cf. Diamond 1973). Broad-gaped birdsfrequently fed on the diminutive fruits of Urera elata(3 mm) as well as the big drupes of B. costaricensis.Below the limit apparently :,et by gape size, most ofthe fruit diameter distributiol!lsin birds' diets resemblethat of the plant community 1LS a whole. However, onlyin the case oftoucanets(Fig. 5d; cf. Fig. 1) was the sizedistribution of fruits eaten s,tatistically indistinguish-able from the distribution of fruit diameters in the plantcommunity (Kolmogorov-SJrnirnov two-sample test;P > .05).

Unbiased data on the rela.tive frequencies of fruitsof different sizes eaten by bil'ds are difficult to collect.I have extensive samples fo:r only two species, man-akins and bellbirds (Figs. 6 and 7). The size distributionof fruit species eaten was sil~ficancly different fromthe size distribution of individual fruits eaten by bell-birds, which fed disproportionately on medium-sizedfruits (Kolmogorov-Smirnovtwo-sample test; P < .01),but this was not so for manakins (P > .05).

Fmit size and s4?ed dispersal

The number of bird specif:s feeding on the fruits ofa particular lauraceous specil~ at Monteverde was in-versely correlated with the di1lmeter of the plant's fruits(Fig. 8; r,= -0.71, n = IS :,pecies in the Lauraceae,P < .01). At least 17 bird s);>ecies, representing eightfamilies and four orders, fed on tIie relatively smallfruits of O. tonduzii, whereas plant species whose fruitswere broader than 1 7 mm attracted no more than fivespecies of birds (Fig. 8). Thesf: results were independentof observation period for plaIJlt species observed at least4 h. For such species, fruit diameter was correlatednegatively with the number of bird species recordedduring the first 4 h of observation watches (r, = -0.61,P < .05; Table I), the total number recorded duringall watches (r, = -0.91, P < .01), and the total fromall watches plus censuses (r, ,= -0.74, P < .01). Therewas no correlation between the total number of birdspecies recorded and either tile number of censuses orthe total observation time per species (r, = -0.18 and0.04, respectively; P > .0S).1'iror was there a correlationbetween the number of bird species observed duringwatches alone (i.e., excluding censuses) and the amountof observation time per plaIJlt species (r, = 0.18, P >.05). Even if such a correlation had been found, theresults presented here should not be biased, becauseneither the amount of observation time nor the numberof censuses was correlated wi1th fruit size (r, = 0.13 and0.23, respectively; P > .05).

Among the 28 additional plant species methodicallystudied (see Study Site and Methods), small-fruitedplant species drew significantly more species of birdsthan large-fruited species (Fi~;. 8; r, = -0.5 I, P < .02).When samples for all plant species studied in detailwere combined, the correlation was slightly higher

offruits than small birds, however (Fig. 4). Maximum(r, = 0.53, P < .001; Fig. 4A) and mean (r, = 0.61,P < .001; Fig. 4B) fruit diameters (as well as lengthsand masses: P < .001) were also correlated with gapewidths for the 32 bird species with five or more feedingrecords. The slope of the linear regression of maximumfruit diameter and gape width (Y = 1.OX + 0.6) re-flects the direct relationship between these two vari-ables. On the other hand, gape width was not correlatedwith diameter of the smallest fruit eaten (r, = -0.10,n = 32 bird species with five or more feeding records;P > .05; Fig. 4A) or with length or mass (P > .05).

Information on the frequencies of fruit species ofdifferent size-classes eaten was available for 10 speciesof birds studied more intensively (Fig. 5). The diets of

814 NATHANIELT. WHEELWRIGHT Ecology, Vol. 66, No.3

'I

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[41

~~

(r. = -0.56, n = 43 plant species, P < .00 I). Fruit massappeared to explain more of the variance (r. = -0.65)than diameter in this case, presumably because it in-corporated the constraining effects of both diameterand length (cf. discussion of B. costaricensis in Obser-vations within Plant Species, above).

cated that birds chose among individual fruits on thebasis of size. Selective feeding b~'I birds was apparentlybased less on deliberately choosing small fruits thanon indiscriminately plucking fruits and being unableto swallow large ones. Foraginl~ toucanets and otherbirds commonly plucked large fiuits of various speciesand spent 1-2 min juggling them in their bills in anobvious attempt to swallow them; often they aban-doned the effort and dropped the fruits (N. Wheel-wright, personal observation). L.arge fruits scarred bybill marks were frequently foun,d below fruiting trees.

DISCUSSION

Seeds collected from seed traps below bellbird,quetzal, and manakin perches, as well as seeds regur-gitated by toucanets foraging at an isolated tree, indi-

June 1985 FRUIT SIZE AND BIRD GAPE WIDTH 815

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rowing snakes (Seib 1981), ~lmivorous mammals (Ro-senzweig 1966), frogs (Toft 1980), lizards (Schoenerand Gorman 1968), plankton-feeding fish (Unger andLewis 1983), sea snakes (VoJis and Moffet 1981), star-fish (paine 1976), stoneflies (Allan 1982). This suggeststhe following generalizations,; (1) the size of the largestprey eaten tends to be directly proportional to the sizeof the predator; (2) larger p):edators consume prey ofa wider diversity and range of sizes and (3) a largermean size than do small predators; (4) the size of thesmallest prey eaten is usuall~, correlated with predatorsize, with small prey often UJlderrepresented in, or ab-sent from, the diets ofiarge p'redators. The slope of therelation between minimum prey size and predator sizevaries (cf. Schoener 1968, VVilson 1975, Paine 1976,Voris and Moffet 1981). ~ltOrs such as baleen whalesor anteaters, specialized to fec~ on clumped, minusculeprey, are notable exceptions.

Interpretations of such pattc:rns, especially lower prey-size limits, derive from foralPng theory. Prey that aresmall relative to a predator ~lTe believed to be ignoredor taken less often than intermediate-sized prey be-cause the difficulty of detection, capture, and/or han-dling increases with diminishing prey size (Storer 1966,Root 1967, Recher and Recher 1968, Schoener 1971,Werner and Hall 1974). Upper size limits or prefer-ences tend to be set by the increases in handling time(Sherry and McDade 1982), risk of injury (Bell 1968),

(2 .1, 6 8 1012141618202224)24

FRUIT DIAMeTER (mm)

FIG. 6. Frequency distribution of mean diameters offruitspecies eaten by Three-wattled Bellbirds (Procnias tricarun-culata), ccmpared with the size frequencies of individual fruitseaten. ..gape width.

N= 844 fruits

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Regardless of the mechanism, the results of size-de-pendent ftuit foraging are likely to be similar from theperspective of the plant. Fruits dropped beneath a plantare hardly more likely to survive than fruits ignoredon the tree, unless secondarily disseminated bya ter-restrial seed disperser.

Bird species with broad gapes consumed more fruitspecies in the Lauraceae than did narrow-gaped species.When all ftuit species are considered, the positivere-lationship between gape width and diet breadth wasnot quite significant for a subsample of well-studiedbirds (although it was significant for 70 bird specieswith at least a single feeding record each: r s = 0.34,P < .01). Broad-gaped birds tended to eat fruit speciesof a larger mean and maximum size, and a larger rangeof sizes. Yet there was no correlation between gapewidth and minimum fruit size, which suggests thatftuit-eating birds differ from more typical predators intheir "prey"-size relationship, as discussed below.

The sizes of "predators" and "prey"

Carnivores representing different taxa commonlyshow similar size relationships to their prey. Birds stud-ied include accipiters (Storer 1966), aerial-feeding pas-serines (Hespenheide 1971), gleaning passerines (Root1967), sandpipers (Holmes and Pitelka 1968), seed-eating finches (Willson 1971), terns (Ashmole 1968),whelk-feeding corvids (Zach and Smith 1981); otheranimals studied include alewives (Brooks 1968), bur-

(2 4 6 8 1012141618 202224 )24

FRUIT DIAMETER (mm)

FIG. 7. Frequency distributiOll of mean diameters of fruitspecies eaten by Long-tailed Manakins (Chiroxiphia linearis),compared with the size fi'equenci,cs of individual fruits eaten.A gape width.

816 NATHANIEL T. WHEELWRIGHT Ecology, Vol. 66, No. 3

or simple physical constraints (Beal and Gillam 1979,Zaret 1980) associated with increasing prey size..

The "prey" of fi"uit-eating birds differ from the preyof carnivores. Because many plants benefit by havingtheir seeds disseminated (Ridley 1930, van der Pijl1969, Howe and Smallwood 1982), most fi"uits whoseseeds are dispersed by birds are not difficult to detector handle (Snow 1971, Wheelwright 1983). Even di-minutive fi"uits are typically easy to find because theymay be brightly colored, aggregated into a conspicuouscluster or compound fi"uit, or set off against contrast-ingly colored associated structures, such as leaves, en-larged bracts, or pedicels (Stiles 1982, Wheelwright andJanson 1985). Despite their size, small fi"uits are noharder to capture than large fi"uits; unlike most animalprey, fi"uits are sessile, non-elusive, and relatively un-defended (Snow 1971; but see Herrera 1982).

The hypothesis that fi"uit-eatingbirds differ from car-nivores in the relationship between body size and foodsize is suggested by the lack of correlation between birdgape width and the minimum size offi"uits consumed,and by the frequency with which large-gaped birds atMonteverde eat very small fi"uits. This hypothesis wouldbe supported if the slope of the relationship betweenbody size and minimum "prey" size were shown to below for these birds, relative to that for typical carni-vores. A review of the foraging literature indicates thatthis is true in most cases, but not in all. For example,Wilson's (1975) general conclusion, based on data inCraighead and Craighead (t956) (see also Storer 1966),that "minimum prey size. ..hardly changes over awide range of predator sizes" is weakened by a closerinspection of the data, particularly when raptors areconsidered by ecological group. Owls, accipiters, fal-cons, and soaring hawks all display an increase in min-imum prey size with body size. The same holds formany other birds (Ashmole 1968, Smith and Temple1982), most other predators cited by Wilson (1975),and some, but apparently not all seed-eating birds(Newton 1967; but see Willson 1971, Rosenberg et al.1982).

1976), which is an advantage for most prey, may be aliability for ftuits because of pl()orer dispersal. Largefruits are more likely to attract fewer seed dispersersand to be dropped uneaten beneath the tree, wheresurvival prospects are low. Thes,e costs are presumablyoffset by the competitive adv2LDtages gained by theseedlings having greater reserves in large s~s (Howeand Richter 1982). Size constraiJllts also affect the sym-metry of interactions between plants and the birds thatdisperse their seeds: large-fruited plants, which are themost specialized in terms of p01:ential seed dispersers,must depend on broad-gaped birds, which are the mostgeneralized in terms of fnrit diet.

Although size is demonstrablly a key characteristicoffnrits, it does not explain the wide variability in thenumber of bird species feeding a1: different plant speciesthat have fruits of the same si2:e (Fig. 8). Part of thevariance is due to sampling biases but the variabilityalso presumably reflects discrimination by birds basedon other fruit attributes. Color showed no consistentrelation to fruit size in the same plant species (Wheel-wright and Janson 1985), and there was no indicationthat nutrient comwsition was strongly tied to size(Wheelwright et al. 1984; but see Herrera 1981). Con-centrations ofN, Mg, K, lipids, ~LDd total nonstructuralcarbohydrates were not correla1ted with fruit mass in23 Monteverde lauraceous species or in II other bird-dispersed species for which I have nutritional data(Spearman rank correlation; P > .05). Plant growthform, commonness, and fecundity, however, unques-tionably influence the number of wtential seed dis-persers for a plant (Wheelwrightet al. 1984). The subtleeffects of many fruit traits in combination will be es-sential in understanding the fora.ging behavior of fruit-eating birds and their coevolution with bird-dispersed

Consequences for seed dispersalThis study suggests that, by producing large fruits,

plants unavoidably exclude narrow-gaped birds andreduce the number of potential dispersers of their seeds.McKey (1975) and Howe and Estabrook (1977) haveproposed that the evolution offruit size is at least partlydetennined by the benefits a plant gains by limiting itsdispersers to a restricted set of reliable, specialized birds.An alternative hypothesis is that fruit size dependsupon seed size, which in turn is determined by the needto store energy and nutrients for seedling establishmentfollowing dispersal (Snow 1971). According to the lat-ter view, large-fruited plants (with correspondingly largeseeds) are actually at a disadvantage with respect todispersal (Wheelwright and Orians 1982), in contrastto the view of McKey (1975). "Escape in size" (paine

MEAN FRUIT DIAMETER (mm)

FIG. 8. Number of bird species observed feeding on fruitsof different plant species as a function of mean fruit diameter.0 15 species in the Lauraceae. 828 sl>ecies from other familiesthat were also studied systematically. x indicates two Ficusspecies whose fruits were eaten pic:cemeal (not included inanalyses).

June 1985 FRUIT SIZE AND BIRD GAPE WIDTH 817

plants. Without adequately controlling first for the ef-fect offruit size, however, it will be difficult to establishwhether birds ignore ti-uits because they are insuffi-ciently nutritious, or simply too big to eat.

ACKNOWLEDGMENTS

C. Guindon, R. LaVal, and especially K. G. Murray kindlyshared feeding records. W. A. Haber and W. Burger identifiedmost of the plant species. Avian specimens were measured atthe Harvard University Museum of Comparative Zoologyand the Yale University Peabody Museum of Natural Historywith the permission and assistance of the curatorial staff: Ithank E. Stevens Wheelwright and F. J. Joyce, Jr., for fieldassistance; the Monteverde community for gracious hospi-tality; G. Russell, B. Marks, and L. Macera for help in pre-paring the manuscript; B. Adams and K. Elliott for help withthe figures; and P. D. Boersma, M. S. Foster, H. F. Howe, C.H. Janson, D. H. Janzen, R. A. Kiltie, E. G. Leigh, Jr., T. E.Martin, G. H. Orlans, T. W. Schoener, J. N. Thompson, S.C. Trombulak, and several anonymous reviewers for theirconstructive comments on previous versions of this paper.This study would not have been possible without generousfinancial aid from the National S~ence Foundation, NewYork Zoolo~ca1 Society, Sigma Xi, and the Frank M. Chap-man Fund, and a Carr Postdoctoral Fellowship from the U ni-versity of Rorida.

q,

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