Co-Occurrences of Foods in Stomachs and Feces of Fruit-Eating Birds

The Condor92:291-303 0 The CooperOrnithological Society 1990

CO-OCCURRENCES OF FOODS IN STOMACHS AND FECES OF FRUIT-EATING BIRDS

DOUGLAS W. WHITE AND EDMUND W. STILB Department of BiologicaI Sciences,Rutgers University,Piscataway, NJ 08855-1059

Abstract. Short-term dietary mixing by American Robins (Turdus migratorius)and other fruit-eating birds in eastern North America was examined using 5,697 records of stomach contents for 11 bird speciesand 3,6 18 avian fecal droppings from New Jersey.Avian seed budgetswere estimated by using fruit morphological data to relate foragingobservations to seed counts from stomachsand feces. Remnants of multiple taxa of foods were found commonly in individual fecesand stomachs although these samples held only 0.25-2 times the seedsconsumed during a typical feeding bout. Depending on bird taxon, seeds from different fruit specieswere mixed in 1.539.6% of feces and 4.2-41.6% of stomachs,and fruit and animal material were mixed in 24-59% of stomachs. Frequencyof mixed seedswas positively correlatedwith proportion of fruit in the stomach and with seed concentration of fruits in the diet. For birds overwintering in the United States,seed mixing in stomachspeaked in winter when birds were most dependent on fruit, not in fall when fruit abundance and diversity were greatest. Thus, estimates of dietary mixing may be biased by seasonalor habitat-related trends in avian fruit dependence or fruit morphology. Furthermore, mixing was no less common in feces than in comparable stomachseven though stomachscontained three to four times more seedmass. This finding along with our observationsof seed treatment by birds suggestedthat mixing was amplified by shuffling of seeds and fruits in the upper gut and by variability of seed transit times through the intestines. Key words: Avian frugivores;feces: fruit; mixed diets;seed dispersal: stomach contents.

INTRODUCTION and White 1982, Johnson et al. 1985, Debussche Diets of fruit-eating bird speciesin the temperate et al. 1987, Herrera 1987), and neotropical birds zone typically include fruits from many plant show preferencesbetween fruit speciesin paired species(Ridley 1930, Martin et al. 195 1, Herrera feeding trials (Moermond and Denslow 1983). 1984a), reflecting the accessibility and simple Nevertheless, reasons exist for individual birds morphology of most temperate fruits. Indeed, in the field to eat fruits of different species(or the mechanismsand selectivepressures for plants insects instead of fruits) in consecutive feeding to “target” fruits for specific bird speciesappear bouts. Birds may seek mixed meals to sample limited (see Herrera 1982a, Janson 1983, Moer- available resources, balance nutrient intake mond and Denslow 1983, Pratt 1983, Gautier- (Berthold 1976a, 1976b; Jordan0 1987, 1988; Hion et al. 1985, Herrera 1985, Wheelwright also seeWestoby 1974) or limit intake of certain 1985) compared to pollen dispersal systems toxins (Herrera 1982a). Mixing may also be re- (Wheelwright and Orians 1982). The broad fruit lated to bird movements becausea bird’s prox- diets attributed to bird speciesresult in part from imity to, and preference for, various foods may lumping dietary recordsacross individuals, hab- change (Levey et al. 1984) when it “fearfully” itats, seasons,and regions(cf. Wheelwright 1986). abandonsa feedingsite (Moore 1978, Howe 1979, Although relevant to questions of avian behav- Pratt and Stiles 1983, Snow and Snow 1984). ior, nutrition, and seed dispersal, little is known Frequent mixing of fruit meals could be sig- about the extent to which individual birds vary nificant for seed-dispersalinteractions in several their fruit diets over brief periods. ways (Herrera 1984a, Stiles and White 1986, Jor- Fruits of different speciesvary in potential nu- dano 1987). Rapid switchesin food use by birds tritional rewards for birds (Herrera 1982b, Stiles might increase the removal rate of low-quality fruits located near high-quality ones (cf. Fleming et al. 1977) and reduce the probability of seeds ’ ’ Received 3 1 March 1989. Final acceptance27 No- being depositedunder parent or conspecificplants vember 1989. where predation and competition would be most

I2911 292 DOUGLAS W. WHITE AND EDMUND W. STILES intense (Janzen 1970, Pratt and Stiles 1983). chosen for study included major North Ameri- Mixed meals may also lead to seeds of two or can frugivores from three families (Mimidae, two more speciesbeing deposited together, which in species;Muscicapidae, six species;and Bomby- turn might affect probabilities of seedpredation, cillidae, one species; Thompson and Willson seedling competition, and, ultimately, plant 1979, Baird 1980, Stiles 1980) and a picid and community structure(Herrera 1988). Finally, dian emberizid species important in New Jersey etary patterns of Mediterranean sylviid warblers field studies (see below, White 1989). Records suggestthat birds lacking accessto a variety of for thesespecies, stored at Patuxent Wildlife Re- fruits necessaryto balance their nutrient intake search Center, Laurel, Maryland, represent a may limit their overall fruit consumption (Jor- fraction of the ca. 250,000 birds collected from dano and Herrera 1981; Jordan0 1987, 1988). throughout North America between 1876-1950 Diversity in the diets of individual birds has in a massive food-habits study designedprimar- been assessedthrough observations of consecu- ily to assessthe impact of wildlife on agricultural tive feeding bouts (Hoppes 1987) and analyses pestsand crops (McAtee 19 12, Beal 19 15, Mar- of stomach (Wheelwright 1986) gut (i.e., stom- tin et al. 195 1). Advantages and shortcomingsof ach plus intestines;Herrera 1984a, Jordan0 1987) the data set were discussedrecently by Wheel- and fecal contents (Sorensen 1981). Inferences wright (1986). The information recordedfor each have also been drawn from seedtrap data (Stiles stomach included collection site and date, stom- and White 1986). Observing consecutive forag- ach fullness and proportion of fruit material by ing bouts in free-ranging, nonterritorial, forest volume, and the identity and, when recorded, birds is difficult and open to observer bias number of seedsof each fruit taxon present.Seeds (Hoppes 1987). The degree of diet mixing re- were enumerated infrequently in the original rec- flected by seedsin guts and fecesdepends on the ords; however, the spotty data apparently reflects bird’s seedbudget, that is, the number of feeding protocol differences among survey personnel bouts and defecations needed to fill and empty rather than a biasing tendency to record only the gut, and the extent to which seedsof different unusual numbers of seeds. speciesare shuffled or retained differentially in Fruit foraging and seed deposition were stud- the gut (Sorensen 1984; Johnson et al. 1985; Lev- ied September through December, 1979-1982, ey 1986, 1987). Diet diversity may be underrep- on three sites in central New Jersey: a mixed- resented by seed contents of guts and feces be- aged woodland (Institute Woods, Princeton), a causelarger, regurgitatedseeds are dischargedby 30- to 50-year-old field with herbaceousand low birds about twice as quickly as smaller, defecated woody vegetation (Franklin Township, Somerset seeds (6-15 vs. 12-50 mitt, respectively; com- County), and a mature oak-dominated woodland bined data from Webber 1895, Nice 194 1, Wals- and adjacent 1- to 20-year-old fields (William L. berg 1975, Herrera 1981, Sorensen 1984, John- Hutcheson Memorial Forest, East Millstone). son et al. 1985). All elsebeing equal, seed-mixing Detailed habitat descriptions were included in frequencies should increase with increasing gut Bard (1952), Horn (1971) Baird (1980) and and fecal volume and decreasingfruit and seed McDonnell and Stiles (1983). In aggregateover size. each fall season, birds used fruits from 20-27 We examine here the extent and variability of plant taxa at each site (White 1989; cf. Baird seedmixing in stomachsof important avian fi-u- 1980, McDonnell and Stiles 1983, McDonnell givores in North America and in autumn fecal 1986). The number of fruits swallowed and the droppings from central New Jersey. arrival-to-departure interval in secondswere recorded for feeding bouts of American Robins METHODS (Turdus migratorius) observed at each site. We compiled data on stomach (i.e., proventric- Seedswere identified to plant speciesin 3,6 18 ulus plus ventriculus) contents for 5,697 indi- avian fecal droppingsand 1,696 regurgitatedseeds viduals from 11 seed-dispersingbird species(see encountered on trails, fallen logs, and ground Table 1 and Fig. 2 for specificepithets and sam- during regular transits of the study sites. Drop- ple sizes)from records of individual assaysorig- pings could be recognizedas originating from (1) inally conductedby the Bureau of Biological Sur- Northern Flickers (Colaptesaura&s), (2) Yellow- vey (later the United States Fish and Wildlife rumped Warblers (Dendroica coronata) or per- Service, Department of the Interior). Bird species haps other Parulinae (Emberizidae), or (3) Amer- MIXED FRUIT DIETS IN BIRDS 293

ican Robins or other mid-sized members of the companying skin and pulp (Levey 1986) and be- Turdinae (Muscicapidae), Mimidae, Bombycil- cause stomach and fecal samples represent only lidae, or Sturnidae based on fecesthickness and a portion of total gut contents. surface texture. We refer here to these dropping To estimate avian seedbudgets, we calculated types as “flicker, ” “warbler,” and “thrush,” re- total fruit mass consumed per feeding bout spectively. A typical full-sized feces from an (number of fruits x individual fruit mass; for American Robin was 20-25 mm long by 4-5 mm American Robins) and total fruit mass repre- in diameter; the end emerging from the cloaca sented by all seeds contained in a stomach or first tended to be widest and was the locus of fecal dropping (here termed fruit mass equiva- urateswhen they occurred.Northern Flicker feces lent) using data on fruit mass and seed number were wider than robin feces,had a well-formed, per fruit for ca. 50 plant speciesin New Jersey grayish, surface layer, and often contained ants; (White 1989). For stomach and fecal samples, warbler feces were narrow and short. The cir- fruit mass equivalent was estimated only when cumstancesand moisture content of the majority seedswere enumerated and fruit mass and seed of fecal droppings suggesteddeposition on the number were known for all plant species. day of discovery; however, many droppings may have been older. To limit biases, we excluded RESULTS evidently disturbed or completely dried droppings and droppings that were of ambiguous or- AVIAN SEED BUDGETS igin. No correction was made for possible dif- American Robins swallowed a median of 0.95 g ferencesin detectability of deposited seeds. of fruits per autumn feeding bout in New Jersey, Although thrush droppings may have been de- the equivalent of three to four typical fruits (me- posited by 10 or more species(White 1989), ob- dian species fruit mass: 0.29 g; Fig. 1A). The servations of birds, dropping locations, and median fruit mass representedby seedsin Amer- dropping phenology suggestedthat our sample ican Robin stomachscollected by the Biological was weighted heavily towards American Robins Survey in autumn in nine northeastern stateswas which foragedfor animal matter on open ground. 1.39 g, similar to the fruit mass eaten in one to Robins were abundant on the study areas pe- two feeding bouts (Fig. 1B). Fruit mass equiva- riodically through late fall. The influence of non- lent of stomach seedsin the whole sample (0.95 robins on thrush feces is uncertain. Most avian g) was less than that in the subsample above frugivores were smaller than American Robins because animal material made up a large pro- and so may have deposited smaller feces with portion of stomach contents in spring (Fig. 2). lower potentials for seed mixing. Nevertheless, Median fruit mass representedby seedsin thrush results from stomach samples (detailed below) fecal droppings examined in autumn in New Jer- suggestedonly an intermediate rate of fruit mix- sey was 0.33 g, or about the mass of a single fruit ing in diets of American Robins. (Fig. 1C). Fruits used by birds in this study con- A bird may expel regurgitated seeds in tem- tained a median of 8.5 seeds per gram of fruit poral and physical proximity approaching that mass (range: 1.6-57.5; see Table 4). of a fecal dropping. However, becausewe could Seeds in the intestines contribute to a bird’s not confidently link individual regurgitated seeds total seed burden. Fresh, whole fecal droppings in the field, we excluded such seedsfrom all anal- known to come from American Robins were 22 ysesof co-occurrencefrequencies. Records of re- -t 12 mm long (mean + SD; range: 15-28 mm; gurgitatedseeds were used only to calculate mean n = 48). Intestines of two salvaged American number of seedsper egestion (see Table 4); for Robins were 230 and 257 mm long. Fecal drop- that analysis, we assumed that seeds were ex- pings may be shapedby the large intestine: ceca- pelled singly by a bird in the thrush category to-vent length in specimentwo was 32 mm. Based based on bird diets, seed size/regurgitation pat- on length, a robin’s intestines might contain 10 terns, and fruit/gape-width restrictions (White fecal loads, equal to the seedsfrom about 3.3 g 1989). of fruit. This is likely an overestimate, however, Seed co-occurrencesexamined here were like- becauseabsorption of nutrients in the small in- ly a conservative estimate of dietary mixing testine should concentrate seeds distally. Eura- (cf. Herrera 1984a, Jordan0 1987) becausebirds sian Blackbirds (Turdus merula) absorb 45-90% sometimes processseeds more quickly than ac- of ingestedpulp dry mass(Sorensen 1984). Thus, 294 DOUGLAS W. WHITE AND EDMUND W. STILES

30 ’ ; INDIVIDUAL FRUITS A

FEEDING BOUTS

FECAL DROPPINGS

4 OL I I I I I 0 1 1 5 6 MASS PER3SAMPLE &, FIGURE 1. Frequencyhistograms of (A) mean species fruit massfor 8 1 native and naturalized speciesin New Jersey(dashed line) and total fruit massconsumed per autumn feeding bout of American Robins in New Jer- sey (n = 266 bouts; solid line), (B) the fruit mass represented by seeds in American Robin stomachs collected year-round throughoutNorth America (n = 22 1 records with seeds enumerated fully; dashed line) or 40 1 from September-December in New Jersey and eight YELLOW- surrounding northeastern states (n = 53; solid line), RUMPED WARBLER iE and (C) fruit mass representedby seedsin thrush fecal mJJASONDJFMAM droppings examined in autumn in New Jersey (n = 2,959 droppings). Triangles indicate medians. MONTH FIGURE 2. Monthly proportions of stomachs with specifiedvolumes of fruit and/or animal matter for 11 on average in American Robins, seeds in a full bird speciesin North America. Individual stomachs contained pure animal (unfilled bars) or fruit (filled gastro-intestinal tract may represent <4 g of fruit bars) matter or a mixture of both. In stomachs with and result from as few as four feeding bouts, or mixed contents, animal (stippled) or fruit (shaded) 13 median-sized fruits. matter predominatedby volume. Sample size is shown Fecal droppings of flickers and warblers con- above each bar; months with five or fewer stomach samples were omitted. Arrows indicate the weighted tained seeds representing about one-third to one- mean percentagefruit volume. fourth the fruit mass equivalent of corresponding stomach samples (medians: 0.34 vs. 0.91 and 0.03 vs. 0.13 g, respectively). bird mass (Spearman’s rank correlation: rs = For the 11 avian fiugivores examined here, 0.945, P < 0.001, n = 11). On average, estimated strong positive correlation existed between the stomach fruit mass was 1.72 + 0.66% of bird mean estimated fruit mass in the stomach and mass. MIXED FRUIT DIETS IN BIRDS 295

TABLE 1. Fruit massequivalents and plant-taxamixing of seedsin stomachsand seedconcentration of fruits in dietsof seed-dispersingbirds. n is numberof stomachswith fruit. Bird speciesdiffered significantly in mean fruit massequivalents (F,, 616= 7.31, P < O.OOOl),mean plant taxaper stomach(F,,,,,,, = 18.61,P < O.OOOl), and mean of log seedsper gram of fruit for eachspecies occurrence in the diet (F,, 39,8= 23.94, P < 0.0001); for thesethree variables, values not sharinga letter are significantlydifferent (Duncan ’s test,P < 0.05). Bird massesare from Clenchand Leberman(1978).

% stomachswith that Fruit mass numberof taxi Bird equivalent Taxa/ Species mass(9) bw) n I 2 3 4 stomach fmYZ~et Gray Catbird Dumetella carolinensis 36.9 60bcd 514 58.4 32.3 8.6 0.8 1.52a 21.8b NorthernMockinabird Mimus polyglotio~ 48.5 97bcd 359 74.1 22.3 3.1 0.6 1.30b 19.0bc Wood Thrush Hylocichla mustelina 47.4 125ab 86 74.4 25.6 1.26bc 16.4bcd Veery Catharusfuscescens 31.2 67bcd 62 77.4 19.4 3.2 1.26bc 21.6b Swainson’sThrush Catharus ustulatus 30.8 34cd 250 78.8 19.2 1.6 0.4 1.24bc 17.2bc NorthernFlicker Colaptesauratus 132.0 154a 419 79.2 18.4 2.4 1.23bc 13.9cde Hermit Thrush Catharusguttatus 31.0 41cd 351 80.1 17.1 2.6 0.3 1.23bc 20.lbc AmericanRobin Turdus migratorius 77.3 135ab 1,085 82.8 15.7 1.6 1.19bcd lO.le Gray-cheekedThrush Catharus minimus 32.8 53bcd 59 84.7 15.3 1.15bcd 11.4e CedarWaxwing Bombycilla cedrorum 33.1 96abc 230 90.0 7.8 1.7 0.4 1.13cd 10.6e Yellow-rumpedWarbler Dendroica coronata 12.6 9d 24 95.8 4.2 1.04d 32.0a

STOMACH CONTENTS for Cedar Waxwings (Bombycilla cedrorum), and Mixing of fruit and animal material. The bird 24% for Yellow-rumped Warblers. Additional speciesexamined relied heavily on fruits (Fig. 2). instancesof animal-plant mixing may have been Except for Yellow-rumped Warblers, the bird missed becauseof rapid digestion of soft-bodied species used fruits in all sampled months in- animals (i.e., earthworms; seeWheelwright 1986) cluding breeding periods, and a majority of birds or rapid regurgitation of large seeds. Stomachs had fruit-dominated diets in over half the bird with animal material exclusively were most com- species-by-monthperiods sampled (range among mon during the spring breeding season. bird species:29-100%). Thrushes that migrate Mixing of fruits from dtflerent species. Frugi- from North America in winter continue to feed vorous birds frequently carried seedsfrom two on fruits and insectsin the neotropics (see Keast or more plant taxa simultaneously in their stom- and Morton 1980). achs (Table 1). Fruit mixing was most common Fruit and animal matter were mixed often in in the Mimidae, in which one-third of stomachs bird stomachs (Fig. 2; cf. Jordan0 1982). The with fruits contained seedsof multiple taxa, and mean percentage of birds with both plant and less common in Turdinae, in which seed taxa animal material in their stomachs, weighted were mixed in only one-fifth of fruit-containing equally for months with five or more records, stomachs. Only 2.5% of fruit-containing stom- was 59% for Northern Flickers, 49% for six species achs (range: O-3.7%) had seedsfrom more than of Turdinae (Veery Catharus jiiscescens through two taxa, and no stomachs had more than four American Robin), 53% for two mimid species fruit taxa. Mean number of taxa per stomachwas (Gray Catbirds Dumetella carolinensis and not significantly correlated with bird mass (rs = Northern Mockingbirds Mimuspolyglottos), 32% 0.345, P > 0.30, n = 11) or mean fruit mass 296 DOUGLAS W. WHITE ANDEDMUND W. STILES

Gray Catbird 2 TABLE 2. Resultsof ANOVAs of fruit taxaper fruit- containingstomach as a function of season(August- ,[oooclo 00 00 Octobervs. November-July)and proportionof fruit 2,r,Nzth;g ;I”’ P;‘ b‘ q _ _ in the stomach(classed as l-50%, 5 l-99%, and 100%) for birdsin North America.

Wood Thrush 2 sourceof variation’ PrOpOr- Inter- ,,oo-_1 Bird tam S~~SOtl tion fruit action Veery 2 Gray Catbird ns * ns - * 61= [. 000 NorthernMockingbird ns ns Swainsons’ Thrush Migrant thrushes ns ns ns 32 NorthernFlicker ns *** ns - &I C0 crooo Hermit Thrush ns ns ns AmericanRobin * ;j Northern Flicker ns ns lu2 CedarWaxwing ns ns ** 5 ~53cIooo~n-- g1- [ I ANOVAs werebased on Type III wms of squares.Number of stom- Hermit Thrush achsper speciesare given in Table I. “Migrant thrushes”lumps data for Veery,,Gray-cheeked Thrush, Swainson’sThrush, and Wood Thrush, 22 long-distancemigrants collected in similar periods(see Fig. 1). ns P > 5 loo-1 oooooo--- 0.05, *P < 0.05, ‘*P < 0.01, *** P < 0.001. E 2 American Robin

,~0~-0-000c3--1 significantly with seasonfor any bird taxon, but Gray-cheeked Thrush 2 it did increase significantly with volume of fruit

1 [ o- in the diet for four bird species.In Cedar Wax- Cedar Waxwing wings, a significant interaction existed between 2 season and relative fruit content, but mixing ,c=loc3--[ ---- tended to be lower in autumn than during the JJASONDJ F M A M rest of the year (1.05 vs. 1.15 taxa per stomach, MONTH respectively). Proportion of fruit in the stomach FIGURE 3. Mean number of fruit speciesper fruit- was negatively (Northern Flicker, Swainson’s containingstomach in monthly samplesfrom 10 bird Thrush Cutharus u.stulutu.s,Hermit Thrush Cu- speciesin NorthAmerica. No barsare shown for months in whichfive or fewerfruit-containing stomachs were tharus guttutus) or insignificantly (other species) collected. correlated with fullness of the stomach. Exami- nation of monthly differences in fruit taxa per stomach showedthat, for birds overwintering in represented by seedsin the stomach (r = 0.273, North America, mixing was highest in winter P > 0.40, n = 1 l), suggestingthat differences (Fig. 3) a period of heavy dependence on fruits among bird speciesin fruit mixing were not due by birds (Fig. 2) in the face of declining numbers simply to differencesin stomach capacity. of fruits per plant as fall-ripening crops are de- Nevertheless,within bird species,stomach fruit pleted. For American Robins, this contrastswith mixing should be expected to increase with the the pattern for total number of insect-plus-fruit quantity of fruit in the stomach and with the taxa per stomach which peaks later in April- diversity of fruit taxa in the environment. In June (Wheelwright 1986). temperate North America, the number of plant specieswith ripe fruits peaks seasonally during CONTENTS OF FECAL DROPPINGS August-October (Thompson and Willson 1979, The frequency of fecal droppings with two or Stiles 1980) while the importance of fruits in bird more individual seedsincreased with bird size diets peaks often in winter (Fig. 2). To separate from 30% in warblers, to 70% in thrushes, to these factors, we examined number of plant taxa 84% in flickers (Fig. 4). The mean number of per stomach by season(August-October vs. No- seedsper dropping increased from 1.4, to 3.9, to vember-July) and proportion of fruit in the 9.2, respectively.The frequencyof droppingswith stomach (l-50%, 51-99%, or 100%) for seven seeds from two or more speciesalso increased bird taxa using analysis of variance (Table 2). with bird size from 1.5% in warblers, to 20.5% Number of plant taxa per stomach did not vary in thrushes,to 39.6% in flickers. Considering only MIXED FRUIT DIETS IN BIRDS 297

70 speciesoccurrences in fecesand stomachsby plant WARBLER taxa. Seed association frequencies in thrush 50 n droppingsvaried widely for 22 plant specieswith adequate data (Table 4). The percentageof seeds of a given speciesthat were depositedwith seed(s) ::f( , , , , of one or more other speciesranged from 1.9- 82.7% and was correlated significantly with the number of seedsper fresh gram of the reference THRUSH fruit (termed fruit seed density; r, = 0.668, P < 1 0.002),but not with the number of seedsper fruit (r, = 0.342, P > 0.10). The mean number of conspecific seeds per egestion was correlated strongly with both fruit seed density (r, = 0.899, P < 0.001) and seednumber per fruit (r, = 0.592, P < 0.01). Thus, besides bird-generated differ- 5- ences, a seed’s depositional fellows also may de- pend on aspects of fruit design including seed and fruit mass and seed number. Similarly, among 13 plant taxa common in September-December in bird stomachs in the northeast (Virginia, Kentucky, Missouri, Iowa, Minnesota, and Ontario and regions to the north and east), 20-60% of taxon occurrenceswere in stomachswith two or more plant taxa (Table 4). .\ 5 15 25 35 45 As in droppings, mixing frequency in stomachs NO. SEEDS PER FECAL DROPPING correlated with fruit seed density (r, = 0.897, P FIGURE 4. Frequencyhistograms of seednumber < 0.001). per fecaldropping for threedropping types examined The fact that mixing frequency varied among in autumnin New Jersey.There were 357 seedsin 260 plant specieswith differencesin fruit seeddensity warblerdroppings, 12,6 13 seedsin 3,219 thrushdrop- suggeststhat variation among bird species in pings,and 1,276 seedsin 139 flickerdroppings. mean number of taxa per stomach may have reflected differences in the types of fruit being multiseeded droppings, the frequency of multi- eaten instead of differencesin dietary mixing per speciesdroppings increased from 4.9%,to 3 1.8%, se. To examine this, we calculated mean fruit to 46.1%, respectively (Table 3). seed density for all taxon occurrencesin stomachs of each bird species(Table 1). Fruit seed MIXING FREQUENCIES FOR INDIVIDUAL density ranged from 0.9455.6 seeds per gram PLANT SPECIES of fresh fruit (median = 13.6, mean = 37.5) in To determine if certain plant specieswere more 64 plant taxa for which we had data (accounting likely than others to occur in mixed-speciessam- for 90.3% of stomach fruit occurrences).Mean ples, we tallied the number of solitary and mixed- seed density of the diet differed significantly

TABLE 3. Frequencydistribution of plant speciesper individual fecal droppingfor three droppingtypes examinedfrom September-Decemberin central New Jersey.Dropping typesdiffered significantly in mean numberof speciesper dropping(F2, 3615 = 41.47, P i 0.0001);each mean was distinct (Duncan ’stest, P < 0.05).

% droppings with that number of species Dwving % multi- Speci~~e~~piw type No. droppings seeded I 2 3 4 Warbler 260 31.2 95.1% 4.9% 1.02 Thrush 3,219 70.0 68.2% 29.01 2.6% 0.2% 1.24 Flicker 139 84.2 53.9% 41.9% 3.4% 0.9% 1.43 298 DOUGLAS W. WHITE AND EDMUND W. STILES

TABLE 4. Associationsamong thrush-depositedseeds in New Jerseyand among fruit taxa in stomachsof 11 bird speciesin the northeast in autumn. n is number of thrush-depositedseeds or number of taxon occurrences in bird stomachs.Plant speciesdiffered significantlyin the probability of a seed being deposited in feceswith a seed of one or more other species(i.e., percentageseeds mixed, F2,, ,3SL)= 68.51, P < 0.0001) and in mean number of conspecific seeds per egestion (fecal droppings plus seeds regurgitated singly; seed numbers log- transformed, F2,,4757 = 123.21, P < 0.0001); for these two variables, values not sharinga letter are significantly different (Duncan’s test, P < 0.05).

Thrush-depositedseeds Stomachs Seedsmixed Conspecific Taxa mixed spy “f$p seeds/egestion Referencetaxon n (%) (X f SD) n f%)

Prunus serotina 1 1.6 64 3.la 1.0 + O.Oa 87 21.8 Cornusjlorida 1 2.2 262 11.5ab 1.1 f 0.3a 117 20.5 Nyssa sylvatica 1 2.3 177 14.lab 1.1 + 0.4a 52 28.8 Lindera benzoin 1 2.7 631 1.9a 1.0 f 0.2a 12 25.0 Viburnumprunifolium 1 2.9 416 17.lbc 1.4 + 0.8ab Cornus amomum 1 4.9 11.6ab 1.9 zk 1.3bcd Viburnum acerifolium 1 5.0 ;z 48.Ofg 1.1 k 0.4a Vitis spp. 1.8 5.1 3,654 28.4cd 2.3 + 1.6cdef 69 40.6 Pyrus sp. 3.2 6.2 87 40.2efg 2.1 k 1.3cde Pellodendronamurense 4.0 6.1 15 46.lfg 2.7 -t 2.3def Cornus racemosa 1 27 44.4efg 1.5 k l.Oab Aronia arbutifolia 2.6 :.: 90 57.8gh 2.7 If: 2.2def Rhamnus catharticus 3.9 14:o 61 61.211 1.8 k 1.4bc Parthenocissusquinquefolia 3.0 17.5 641 31.7de 2.7 f 2.2efg 54 44.4 Ilex verticillata 5.8 20.9 29 51.7 Celastrusorbiculatus 4.8 21.9 710 3 1.4de 3.8 + 3.2gh Phytolaccaamericana 9.5 24.1 2,779 29.3cd 7.8 + 7.3i 61 45.9 Juniperusvirginiana 1.2 26.6 1,512 52.6fg 3.2 + 2.5fgh 23 30.4 Myrica pensylvanica 1 33.2 216 48. lfg 4.2 + 3.9gh 10 60.0 Rosa multijlora 4.6 38.6 1,010 28.8cd 7.3 f 5.5i Toxicodendronradicans 1 45.1 414 53.Ofg 4.1 f 4.9h 42 52.4 Sambucuscanadensis 3.8 47.8 30 60.0 Lonicerajaponica 6.1 48.2 312 82.7i 4.2 k 4.8h Rhus spp. 1 51.5 69 33.3de 3.0 k 4.Ocde 28 53.6

among bird species (Table 1; data log-trans- in shrubby habitats, and low for Gray-cheeked formed) even when distinctly narrow-gaped Yel- Thrushes, many of which were collected from low-rumped Warblers were omitted from the forests in autumn (cf. Fig. 2 and Martin et al. analysis (1$9,X89, = 25.61, P < 0.0001). Further- 1951). more, significant positive correlation existed between fruit seeddensity in the diet and taxa mix- DISCUSSION ing in the stomach (rs = 0.758, P < 0.05), supporting the idea that mixing was food biased. BIRD DIETS Fruits with single, large seeds(e.g., Prunus, Cor- Seeds from different plant species were mixed in nus, Nyssa) were recorded often in diets of bird high frequency in stomachs and feces given the specieswith low mixing, while fruits with mul- small volume of these samples in relation to the tiple small seeds (e.g., Rubus, Sambucus, Vuc- quantity of fruit consumed in a typical single- cinium, Ilex) were common in diets of bird species species foraging bout. Plant and animal material with high mixing. Becauseseed size varies with were similarly highly mixed in stomachs. Co- season and habitat (Stiles 1980), differences occurrencesof fruits in guts of nontropical, fruit- among bird speciesin stomach mixing rates may eating birds may be common. Eight bird species reflect temporal sampling biasesand bird habitat examined in Spanish scrublands contained seed preferences.Thus, mixing was high for Gray Cat- or skin of 1.33-2.43 plant speciesper whole-gut birds, many of which were collected in summer sample (Herrera 1984a, Jordan0 1987). In con- MIXED FRUIT DIETS IN BIRDS 299 trast, “very few” of the ca. 775 fruit-containing fecesof British thrushes had mixed fruit species -11 B . . . . (Sorensen 198 1, p. 246). 1 Co-occurrence of foods in stomachsand feces 1 was not a sure measure of mixed meals (i.e., 2 -I=++ consumption of different foods in consecutive Z* feeding bouts) for three reasons. First, mixing + +--===+- frequencieswere affectedby simple physical con- siderations, including stomach and dropping - ...... + . . .. volume, proportion of stomach contents in fruit, .. . t and fruit size and seednumber (Stiles and White 1986). Similar relationships existed for sylviid 0 60 120 warblers in Spain where the number of fruit TIME ELAPSED (mid speciesper gut was positively correlatedwith bird FIGURE 5. Retention times for seeds of Sassafras mass and percentage fruit in the gut (Jordan0 albidum(solid lines) and Lindera benzoin(dotted lines) 1987). Small bird size may also affect mixing eaten by a Veery during three 2-hr feeding trials in an indoor flight cage. The interval from drupe ingestion indirectly through gape-sizelimitation of dietary to seed regurgitation and expulsion or to the end of diversity (Wheelwright 1985, Jordan0 1987). observation (arrowhead) for each fruit is represented This effect may be accentuated here becausethe by a horizontal line; for clarity, lines are offset within Yellow-rumped Warbler, the smallest frugivore each trial. Crossbarsindicate a fruit was visible for l- examined, also specializes on a few species of 10 set when it was regurgitatedinto the bill and reswallowed. Fruit skins had been painted contrasting waxy fruits (White 1989). A likely result of these colors to allow identification of reappearing fruits. physical biases is that avian food habitat studies Where seed fates were ambiguous,we assumed seeds based on plant speciesoccurrences in stomach, were expelledin ingestionorder (seeLevey 1987). Note gut, or fecal samples will emphasize small- over that misinterpreting the origin of a regurgitatedseed as the most recently consumed fruit would result in a large-seededfruits. seriousunderestimate of seed retention time. Second, overestimation of fine-scale mixing in the diet may have resulted when slow-passing seedsor animal hard parts were mixed with recently eaten, fast-passingfood. Seedtransit times Fruits and seeds may also be shuffled from through vertebrate guts often have skewed dis- ingestion order by gizzard contractions and peri- tributions with long tails (e.g., Hoelzel 1930, stalsis in the upper gut. In a captive Veery, we Ridley 1930, Proctor 1968, Janzen 1981, Levey observedthat swallowed marked fruits with firm, 1986, Braun and Brooks 1987). Thus, even in oily pulp (cf. Stiles 1980) were often regurgitated small passerinebirds feeding on fruits of a single into the bill, reswallowed, and transferred to the species,the slowest-passingseed was retained a gizzard for separation of pulp and seed;the clean median 3.1 times longer than the fastest-passing seeds,en route to being expelled, then passedby seed (range: 1.7-11.1, IZ = 15 bird species;data recently eaten fruits (Fig. 5; also seeLevey 1987). assembledfrom Webber 1895; Nice 194 1; Wals- We also saw fruits regurgitated and reswallowed berg 1975; Herrera 198 1; Levey 1986; White and in a Gray Catbird and American Robins in cap- Stiles, unpubl. data). Some insect parts may also tivity and a Gray-cheeked Thrush (Catharus pass slowly (Jordan0 and Herrera 1981). Over- minimus) and robins in the wild. Although such lapping transit times may account for the fact “juggling” may arise simply from the difficulty that fruit mixing appeared no less common in of distinguishing internally between firm fruits feces than in stomachs although stomachs con- and seedsdestined for expulsion, it shows how tained three to four times more seedmass. Vari- readily seedsmight be mixed in the upper gut. ation in transit intervals may arise from differ- Finally, observed mixing frequencies were a ences in seed size and processing mode (i.e., function of additional unquantified factors in- regurgitation vs. defecation; Sorensen 1984, Lev- cluding the birds’ overall diet breadth and local ey 1986) pulp texture and adherenceto the seed spatial and temporal patterns of fruit availabil- (Levey 1986), and seed specificgravity and sur- ity. face area (Hoelzel 1930, Janzen 198 1). Why do birds mix their diets as much as they 300 DOUGLAS W. WHITE AND EDMUND W. STILES do? A prevailing view is that mixed diets reflect AVIAN SEED DISPERSAL selective feeding to balance nutrient intake (Bo- naccorso and Gush 1987; Jordan0 1987, 1988; For plants, there may exist a high premium on Herrera 1988) or minimize effects of food-spe- seeddispersal: it may allow seedsto escapepre- cific poisons and digestion inhibitors (Howe and dation and competition near parent and conspe- Vande Kerckhove 1980, Herrera 1982a, Janzen cific plants, and it may increase the chance seeds 1983). The regularity with which insectsand fruits will colonize sites favorable for plant regenera- were mixed in bird stomachs bolsters the idea tion (seeHowe and Smallwood 1982, and Janzen that fruits are a readily accessiblesource of cal- 1983 for reviews). The consumption by birds of ories but an inadequate sourceof protein for most fruits of different species,or fruit and insects, in birds (Rowan 1967, Jordan0 and Herrera 198 1, temporal proximity might influence fruit remov- Jordan0 1982, Wheelwright 1983, cf. Milton al rates, seed distribution patterns, seed preda- 1979, Mattson 1980). Mixed diets may also re- tion, and seedling competition. flect a need for balanced uptake of minerals (cf. First, mixing of fruit meals will result in a Bennetts and Hutto 1985, Johnson et al. 1985, degree of temporal overlap in dispersal periods Roze 1985, Herrera 1987), vitamins, carot- of concurrently available fruits. Thus, within a enoids, and water (Herrera 1982a, 1982b; De- habitat and range of fruit quality, fruits with low busscheet al. 1987). Fruit pulp furthermore var- avian preferencerankings (cf. Martin 1985) may ies in plant secondarycompounds (Herrera 1982a have removal chronologies and spatial dissem- and included citations) and degradation products ination patterns (but not absolute removal rates) (Janzen 1977; Eriksson and Nummi 1982; but that parallel strikingly thoseof high-ranking fruits, seeHerrera 1984b, 1985) that may also promote at least while crops of the latter speciesremain mixing in bird diets. (Fleming et al. 1977). So it may be advantageous Notwithstanding thesenutritional factors,bird for specieswith low-quality fruits or small fruit movement coupled with weak preferencesamong crops to mature fruits in synchrony with those similar fruits may provide a simple alternative of other speciesin the community (cf. Herrera explanation for mixed-fruit meals. During au- 1988). tumn and winter, standing crops of ripe fruits on Second, dispersal of seedsaway from conspe- individual plants often exceed the meal size of cifics is a likely by-product of dietary mixing in individual birds (Stiles 1980), yet birds charac- birds. In Papua New Guinea, Pratt (I 983) found teristically feed in distinct short visits to fruit that omnivorous birds of paradise may deposit patches (Herrera and Jordan0 198 1, Sorensen a smaller fraction of seeds under fruiting trees 1981, Jordan0 1982, Paszkowski 1982, Snow and than do entirely frugivorous fruit-pigeons and Snow 1986, Hoppes 1987). Birdssometimesleave bowerbirds. In the current study, American Rob- fruiting plants when they fall from precarious ins and Northern Flickers foraging for insects feeding perches (Janzen 1983, Moermond and often deposited seedsin open areas that may be Denslow 1983) or are chased by fruit defenders superior regeneration sites(also seeSmith 1975). (Moore 1978, Merritt 1980, Pratt and Stiles 1983, It seems unlikely, however, that fruit traits that Snow and Snow 1984) or competitors (Herrera may promote mixed diets evolved because of and Jordan0 198 l), but short visits appear most- selection for wide seed dispersal. Instead, traits ly to be part of a suite of traits that reduce a such as unbalanced pulp nutrients and toxins bird’s risk of predation (Howe 1979, McDonnell more likely reflect plant nutrient constraints or 1986, Snow and Snow 1986). Often birds take adaptations to deter nondispersing fmgivores only a fraction of a full-sized meal before leaving (Herrera 1982a). a patch (e.g., Fig. l), and in their first postforaging Finally, seedsmixed with fecal droppings may move, they may avoid fruiting, conspecificplants interact to influence seedpredation rates or seed- (Herrera and Jordan0 198 1, Jordan0 1982, ling competition. From a plant’s perspective,seed Hoppes 1987). Thus “fearful” movements (sen- associations in bird feces were nonrandom but su Howe 1979) away from one plant may place highly variable: number of conspecificseeds per a hungry bird near fruits of different species,and dropping and frequency of mixing in droppings the simple proximity of these latter fruits may increased with bird size and fruit seed density increasetheir attractiveness(Fleming et al. 1977, (seedsper unit wet fruit mass).However, for seeds Levey et al. 1984). attractive to vertebrates (e.g., Prunes), risk of MIXED FRUIT DIETS IN BIRDS 301

predation for individual seedsmay not increase DEBUSSCHE,M., J. CORTEZ,AND I. RIMBAULT. 1987. when seedsare aggregatedin a dropping if ani- Variation in fleshy fruit composition in the Med- mals eat all seeds they encounter (Webb and iterranean region: the importance of ripening season, life-form, fruit type and geographicaldistri- Willson 1985). Additional experiments are need- bution. Oikos 49~244-252. ed to determine if seedcomposition of droppings ERIKSSON,K., AND H. NUMMI. 1982. Alcohol accu- influencesdetectability or predation risk for seeds mulation from ingested berries and alcohol me- that are comparatively unattractive to predators. tabolism in passerinebirds. Omis Fenn. 60:2-9. FLEMING,T. H., E. R. HEITHAUS,AND W. B. SAWYER. The duration of closephysical associationamong 1977. An exnerimental analvsis of the food lo- seedsdeposited in a single dropping is uncertain. cation behavior of fiugivorous bats. Ecology 58: Secondarydispersal by rain, frost heaving, seed- 619-627. caching animals, incidental animal activity, or GAUTIER-HION,A., J. M. DUPLANTIER,R. Quats, F. other factorscan separateseeds (Livingston 1972, FEER,C. SOURD, J. P. DECOUX, G. DUBOST,L. EMMONS, C. ERARD, P. HECKETSWEILER,A. Smith 1975, Janzen 1982). Moreover, seed as- MOUNGAZ~,C. ROUSSILHON,AND J. M. THIOLLAY. sociations in a given patch in autumn are a dy- 1985. Fruit charactersas a basis of fruit choice namic function of disperserinput and predation and seed dispersal in a tropical forest vertebrate (Stiles and White 1986); seed dormancy is com- communitv. Oecoloaia 65:324-337. HERRERA,C. M. 1981. -Are tropical fruits more re- mon among northeastern plants (U.S. Depart- warding to dispersersthan temperate ones?Am. ment of Agriculture, Forest Service 1974). Thus, Nat. 118:896-907. predation probabilities may vary with seed den- HERRERA,C. M. 1982a. 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