The Condor 102:66‘-672 0 The Cooper Ornithological Society 2ooO

WINTER FLOCKING OF INSECTIVOROUS IN MONTANE - FORESTS IN MIDDLE AMERICA ’

DAVID I. KING USDA Forest Service Northeastern Research Station, University of Massachusetts, Amherst, MA 01003, e-mail: [email protected]

JOHN H. RAPPOLE Smithsonian Conservation and Research Center, 1500 Remount Road, Front Royal, VA 22630

Abstract. We studiedmixed- insectivorous flocks in pine-oakforests in Mid- dle America during three winter seasonsto determine whether patterns of flock structure and dynamics were similar to those reported from other tropical sites. We also analyzed patterns of associationamong bird species, as well as their foraging behavior and the veg- etation characteristicsassociated with birds in flocks. We encountered333 flocks containing 144 species,of which 26 specieshad adequatesample sizes for analyses.The size and rate of movement of the flocks were similar to those reported from other Neotropical sites, however, the species richness of our flocks was lower than reported in most other studies, perhaps due to simpler vegetation structure or higher latitude. Only 3 of 50 significant correlationsbetween speciespairs were negative, indicating that speciesgenerally were not restrictedin their participationin mixed-speciesflocks by other species.In only one instance did we observe correspondencebetween the associationof species-pairsin flocks and their foraging behavior. For most speciesthere was no relationship between associationbetween species-pairsin flocks and vegetation parameters with which they were associated.Thus, additional factors besides foraging facilitation and mutual associationwith particular vege- tation characteristicsmust be responsiblefor many of the positive correlationsamong species pairs. We suggestthat non-random associationamong species within flocks may result in part from enhancedvigilance for predatordetection afforded by flock membersusing similar parts of the environment at the same time. Key words: foraging, mixed-species jfocks, Neotropics, vegetation characteristics.

INTRODUCTION suiting in intimidation or deterrence of some Participation by birds in mixed-species flocks is predators by mobbing (Moynihan 1962). “For- widespread in the Neotropics, and numerous aging enhancement” hypothesesinclude (1) “in- studies have been directed at determining the formation transfer” in which flock members adaptive significance of this behavior (Powell benefit from clues provided by flock mates about 1985). Explanations for the phenomenon fall the location of resources(Moynihan 1962, Ward into two principal categories: reduced predation and Zahavi 1973, Valburg 1992), (2) the “beat- and enhanced foraging success. er” effect in which flock members exploit prey The “predation reduction” category of flock- flushed by the activity of the flock (Moynihan ing benefits includes the following explanations: 1962, King and Rappole, in press), and (3) re- (1) enhanced detection of a potential predator duction in foraging niche overlap among flock through monitoring behavior of co-participants participants (Morse 1970). (Moynihan 1962, Pulliam 1973, Powell 1985), In addition to benefits, several researchers (2) reduced exposure to predation by being part have proposedthat there are costs involved with of a group (“distraction” hypothesis of Miller participation in mixed-species foraging flocks as 1922 and Moynihan 1962; “selfish herd” of well. For instance, increased competition for Hamilton 1971 and Vine 197 l), (3) capitaliza- food, or reduced foraging efficiency as a result tion by some members on superior familiarity of of the necessity to modify foraging behavior to other flock members with the flock’s home match the speed or location of the flock could range, thereby avoiding dangerous areas (Moy- have negative effects on flock members, forcing nihan 1962), and (4) “strength in numbers” re- them to make choices in terms of participating in flocks or foraging as solitary individuals ’ ’ Received22 November1999. Accepted12 April (Jones 1977, Hutto 1988). 2000. The study of the costs and benefits of flock

[6641 MIXED-SPECIES BIRD FLOCKS IN MIDDLE AMERICA 665 participation and their effect on flock composi- January-15 February 1997; 10 January-23 Feb- tion is complicated by the fact that flock partic- ruary 1998) primarily in the central and western ipants may benefit simultaneously from en- highlands of Honduras and the eastern highlands hanced predator detection and enhanced forag- of Guatemala. We also include data from four ing efficiency (Moynihan 1962, Powell 1985). days of fieldwork in Chiapas, Mexico (28 Feb- For example, flocking could improve foraging ruary-3 March 1998). We concentrated our field efficiency because flock members spend less efforts in pine and pine-oak habitat above 1,000 time scanning for predators (Sullivan 1984, El- m elevation. Other major habitat types in the gar 1989). Also, it is probable that different highlands are broadleaf forest (including cloud kinds of flocks may provide different benefits to forest), pasture, agricultural fields (sun coffee, their members (Moynihan 1962). Clearly, addi- beans, corn), tree crops (bananas, shade coffee, tional information is needed on patterns of as- citrus), and various early successionalstages of sociation of species within and among flocks forest regrowth. The bird specieswe included in that allow us to test hypothesesabout the costs our analyses are widespread and abundant in and benefits of flocking (Powell 1985, Hutto pine and pine-oak forest across the study area 1994, Latta and Wunderle 1996). (Howell and Webb 1995), thus we are confident Previous studies of mixed-species foraging that our results were not significantly affected flocks in the Neotropics indicate that there is by regional variation in bird distribution and substantial regional variation in the composition abundance. and dynamics of mixed-species flocks. In the hu- Flocks were located by walking through for- mid tropics, resident species tend to predomi- ested habitats searching visually for individual nate, and many individuals occur outside of birds and listening for vocal members of mixed- flocks (Powell 1985). These characteristicscon- species flocks, such as the Greater , trast with those observed for flocks in highland Dusky-capped Flycatcher, and Painted Redstart pine and pine-oak forests in Mexico (Hutto (scientific names of bird speciesare listed in Ta- 1987, Gram 1998) and the Caribbean (Latta and ble 1). A flock was defined as > 2 individuals Wunderle 1996) in which Neotropical-Nearctic within 25 m of each other and moving in concert migrants play a much greater role, and fewer (Hutto 1987). When a flock was located, the ob- individuals occur away from hocks. We studied server stayed with it until no further bird species mixed species flocks in southern Mexico, Gua- were detected. Average time required to record temala, and Honduras to determine whether pat- all species in a mixed-species flock was about terns of flock structureand dynamics in this little 1.5 hr, although it ranged up to 4 hr, depending studied habitat were similar to those reported on flock size and habitat conditions. Although from other parts of the tropics. In addition, we birds were not individually marked, we are con- tested whether bird species were nonrandomly fident few species joined or left the flocks as associated with other species, whether positive they progressedbecause few of the species in- or negative relationships among specieswere as- cluded in our analyses occurred out of flocks on sociated with similarities or differences in for- a regular basis (see below). We tested for non- aging behavior, and whether there was evidence random association among species by scoring of intraspecific interactions or sex-specific dif- speciesas present (1) or absent (0) in each flock ferences in foraging behavior within flocks. Fi- and analyzed the association among species us- nally, because previous studies have cited the ing Pearson correlation, which, when applied to possible confounding effects of the association 0, 1 data, yields a correlation coefficient, the P- of species with specific vegetation characteris- value of which corresponds to that of a Chi- tics in analyses of mixed-species flocking (Hutto square test of independence (Sokal and Rohlf 1994, Latta and Wunderle 1996), we also quan- 1995). Significance values were Bonferroni-cor- tified vegetation variables to test whether asso- ciations of species with particular vegetation rected to account for multiple tests. These anal- characteristicsmight be responsible for positive yses were restricted to species that occurred in or negative relationships between bird species. 2 15% of flocks, plus the Red-faced Warbler because sufficient foraging data were available METHODS for this species (see below). Field work was conducted over three winter sea- We tested whether species were represented sons (1 December 1995-1 February 1996; 10 in flocks as solitary individuals more often than 666 DAVID I. KING AND JOHN H. RAPPOLE

TABLE 1. Frequency and average (2 SE) number of individuals per flock for bird species occurring in 2 15% of flocks, or species for which 2 10 foraging maneuvers were recorded, in CentralAmerica and Mexico, 1995- 1998. Average numbers of individuals per flock was calculated for flocks in which the species occurred.

Frequency of Mean number of occurrence individuals

Wilson’s Warbler (Wilsonia pusilla) 81.7 1.41 t 0.05 Black-throatedGreen Warbler (Dendroicu virens) 77.5 3.10 f 0.15 Blue-headed Vireo (V&o soliturius) 63.1 1.22 2 0.04 Hermit Warbler (Dendroicu occidentulis) 61.3 2.50 2 0.11 Black-and-white Warbler (Mniotilita van’u) 56.5 1.11 ? 0.03 Townsend’s Warbler (Dendroicu townsendi) 54.4 1.62 2 0.07 Painted Redstart (Myioborus pictus) 53.5 1.34 ? 0.04 Grace’s Warbler(Dendroicu gruciu) 49.9 1.36 ? 0.05 Slate-throated Redstart (Myio%orus miniutus) 47.5 1.30 t 0.04 Olive Warbler(Peucedrumus tueniutus) 42.9 1.35 + 0.04 Golden-cheeked Warbler (Dendroica chysopuriu) 39.9 1.14 t 0.03 Crescent-chested Warbler (Vermivoru superciliosu) 39.6 1.67 2 0.06 Greater Pewee (Contopus pertinun) 39.0 1.18 t 0.04 Hammond’s Flycatcher (Empidonux hummondii) 27.9 1.01 ? 0.03 Dusky-capped Flycatcher (Myiarchus tuberculifer) 26.4 1.23 ? 0.03 Brown Creeper (Certhiu americana) 24.9 1.23 2 0.03 Streak-headed Woodcreeper (Lepidocoluptes ujjinis) 24.6 1.23 2 0.03 Hepatic Tanager (Pirungu &vu) 23.7 1.34 ? 0.04 Tufted Flycatcher (Mitrephunes phueocercus) 20.4 1.24 +- 0.03 Acorn Woodpecker(Melanerpes formicivorus) 18.6 2.08 ? 0.06 Mountain Trogon(Trogon mexicanus) 17.7 1.31 rt 0.03 Golden-wingedWarbler (Vermivoru chrysopteru) 17.7 1.00 ? 0.02 Common Bush Tanager (Chlorospingus ophthalmicus) 16.5 5.02 2 0.17 Black-headed Siskin (Curduelis notutu) 16.2 2.50 ? 0.10 Hairy Woodpecker (Picoides villosus) 15.3 0.96 ? 0.02 Red-faced Warbler (Curdellina rubrifrons) 12.0 0.98 t 0.02 expected by chance by comparing the frequency maneuvers in which a bird must leave its perch of flocks that contained only a single individual to reach food). Few aerial maneuvers were di- of a species with the expected frequency calcu- rected at the inner portion of the plant, so only lated using a Poisson distribution. In addition, one category of aerial maneuver was considered. we tested whether more flocks containing two or We analyzed the distribution of foraging maneu- more individuals had individuals of both sexes vers by each species, and the distribution of for- (based on plumage type) more than expected by aging maneuvers between sexes for dimorphic chance using sign tests. species, among the three categories using Chi- Foraging behavior was sampled by observing square tests of independence. Although analyses focal individuals, and recording the first forag- of foraging behavior were restricted to species ing maneuver observed. Although the use of ini- for which we recorded > 10 foraging maneu- tial foraging observations may bias results to- vers, the average number of foraging maneu- wards conspicuous foraging maneuvers, these vers/specieswas much higher than this (see be- biases appear to be minor in most cases(Wagner low). 1981, Morrison 1984, Hejl et al. 1990). Only In addition, vegetation data were collected at one foraging maneuver for each species per five randomly-located points along 42 l-km flock per individual was recorded to ensure in- transects on which flock species composition dependence of observations. We classified for- and bird foraging behavior also were recorded. aging behaviors into three categories: (1) near Vegetation parameters measured included cano- perch foraging maneuvers (foraging maneuvers py height, number and size (dbh) of trees by directed at food that can be reached from the species,shrub density, canopy cover, and ground bird’s perch) in the inner half of the plant, (2) cover (James and Shugart 1970). These vari- near perch foraging maneuver in the outer half ables were averaged for each transect, tested for of the plant, and (3) aerial maneuver (foraging normality using Shapiro-Wilk tests, and log- MIXED-SPECIES BIRD FLOCKS IN MIDDLE AMERICA 667 transformed where necessary to improve nor- after dawn in a manner consistent with behavior mality and equality of variances. We calculated directed at assembling the flock for the day’s correlation coefficients between the number of activities. Flock members apparently do not individuals of each bird specieson each transect roost together. In one instance, a Painted Red- and vegetation variables measured on each tran- start was found calling loudly alone, evidently sect using Pearson correlation. Only bird species preparing to roost on a horizontal root sticking for which we analyzed foraging behavior were out from an overhanging road cut just before included in this analyses. We reduced the di- dusk. A pile of droppings below the spot indi- mensions of the vegetation variables using prin- cated that this roost had been in use for some cipal components analysis (PCA), rotated the re- time. In another instance, two Tufted Flycatch- sulting PCA axes using Varimax rotation, and ers, also frequent nucleur species, were found ordinated all bird specieson the first two rotated calling loudly just before dusk with no other vegetation factors. Statistical tests are consid- flock members evident. On one occasion, we ob- ered significant at P < 0.05 unless stated oth- served the pre-dusk movement of an entire flock erwise, and were Bonferroni-corrected where to a water source for bathing. On several occa- necessary to account for multiple tests. Means sions, flocks approaching from different direc- are presented -C SE. tions were observed to merge together. No evi- dence of overt aggressiveor territorial behavior, RESULTS e.g., chases or supplantings, were observed, al- We detected 6,695 individual birds of 144 spe- though these occurrences often were accompa- cies in 333 flocks during the course of the study. nied by evident increased levels of vocalization. Flock size averaged 20.4 2 0.6 individuals, and on average 12.6 -C 0.5 specieswere represented. RELATIONSHIPS AMONG SPECIES Twenty-five species occurred in > 15% of The correlation analyses revealed 47 significant flocks, and were included in the analyses (Table positive correlations out of 338 possible com- 1). In addition to these, we included a 26th spe- binations of speciespairs. Wilson’s Warbler was cies, the Red-faced Warbler, which occurred in correlated with Slate-throated Redstart. Black- 12% of the flocks that we observed, because we throated Green Warbler was correlated with had sufficient foraging data (> 10 maneuvers). Blue-headed Vireo, Black-and-white Warbler, Painted Redstart, and Grace’s Warbler. Blue- FLOCK STRUCTURE AND DYNAMICS headed Vireo was correlated with Townsend’s Few individuals of any insectivorous bird spe- Warbler. Hermit Warbler was correlated with cies were observed out of flocks, except for the Townsend’s Warbler, Painted Redstart, Olive, dawn (to 30 min after sunrise) and dusk (30 min Golden-cheeked and Crescent-chestedWarbler, before sunset) periods during which flocks were Greater Pewee, and Brown Creeper. Black-and- assembling or breaking up for the night, respec- white Warbler was correlated with Townsend’s tively. Generally, flocks appeared to be cohe- and Crescent-chestedWarblers and Greater Pe- sive, and moved within a restricted area corre- wee. Townsend’s Warbler was correlated with sponding to a home range. Straight-line distanc- Slate-throated Redstart, Golden-cheeked and es traveled were used to calculate approximate Crescent-chestedWarbler, Greater Pewee, Tuft- size of the home range for four flocks. Assuming ed Flycatcher, Mountain Trogon, and Red-faced that home ranges were roughly circular, esti- Warbler. Painted Redstart was correlated with mates were 1.8, 3.1, 7.1, and 9.6 ha. Because Grace’s Warbler, Greater Pewee, Acorn Wood- flocks rarely were followed for more than a few pecker, and Black-headed Siskin. Grace’s War- hours before a full count of species was ob- bler was correlated with Greater Pewee and He- tained, these likely represent minimum home patic Tanager. Slate-throated Redstart was cor- range size estimates. related with Golden-cheeked and Crescent- Flocks appear to form shortly after dawn, and chested Warbler, Spot-crowned Woodcreeper, on several occasions, Painted Redstarts, a con- and Common Bush-Tanager. Olive Warbler was spicuously-colored, noisy bird that exhibited the correlated with Golden-cheeked and Crescent- characteristicsof a nucleur species (sensu Moy- chested Warbler, Greater Pewee, Hammond’s nihan 1962), were observed alone calling loudly Flycatcher, Brown Creeper, and Tufted Flycatch- and flashing their wing and tail patches shortly er. Golden-cheeked Warbler was correlated with 668 DAVID 1. KING AND JOHN H. RAPPOLE

TABLE 2. Foraging behavior of 12 bird species in mixed-species foraging flocks in Central America and Mexico, 1995-1998. Values that differ significantly from expected values are in bold print. Foraging maneuvers are defined in the text.

Foragingmaneuver Near perch Near perch Bird species Aerial inner outer X2 P n Wilson’s Warbler 15 8 5 7.3 0.03 28 Black-throated Green Warbler 11 11 11 0.0 1.00 33 Blue-headed Vireo 8 6 6 0.0 0.99 20 Hermit Warbler 8 11 15 1.2 0.56 34 Black-and-white Warbler 1 21 4 61.1

Crescent-chested Warbler. Crescent-chested foraging maneuvers were significantly noman- Warbler was correlated with Spot-crowned domly distributed among foraging categories Woodcreeper, Tufted Flycatcher, and Red-faced (x2*4 = 149.3, P < 0.001). Black-and-white and Warbler. Greater Pewee was correlated with He- Crescent-chested Warblers used aerial maneu- patic Tanager. Spot-crowned Woodcreeper was vers significantly less than expected by chance. correlated with Common Bush-Tanager. Tufted Wilson’s Warblers, Slate-throated Redstarts,and Flycatcher was correlated with Red-faced War- Red-faced Warblers used aerial maneuvers more bler. Acorn Woodpecker was correlated with than expected by chance. Black-and-white War- Hairy Woodpecker. We also observed three spe- blers used near-perch maneuvers directed at the cies pairs that were negatively correlated: Tufted inner portion of the plant significantly more than Flycatcher and Black-throated Green Warbler, expected by chance, and Golden-cheeked War- Common Bush-Tanager and Greater Pewee, and blers used near-perch maneuvers directed at the Hepatic Tanager and Slate-throated Redstart. inner portion of the plant significantly less than The ratio of positive to negative correlations was expected by chance. Grace’s, Olive and Cres- significantly different than that expected by cent-chested Warblers used near-perch maneu- chance (sign test; P < 0.001). vers directed at the outer portion of the plant Twenty-three of the 26 bird species that oc- significantly more than expected by chance, and curred in 2 1.5% of flocks were represented Slate-throated Redstartsused near-perch maneu- within flocks by a single individual significantly vers directed at the outer portion of the plant more often than expected by chance based on significantly less than expected by chance. The the Bonferroni corrected P-value (P = 0.002). foraging maneuvers of Black-throated Green The frequency with which Hermit Warblers, Warblers, Blue-headed Vireos, Hermit Warblers, Common Bush-Tanagers, and Black-headed Sis- and Townsend’s Warblers did not differ among kins occurred in flocks as sole representativesof foraging categories (P 2 0.12). Foraging behav- their species did not differ from random. The ior did not differ between male and female two sexually dimorphic species for which we Black-and-white and Golden-cheeked Warblers have data (Golden-cheeked Warbler and Black- (P > 0.30), the two sexually dimorphic species and-white Warbler) were represented by mem- for which we have sufficient foraging data. bers of both sexes(based on plumage type) more Several of the vegetation variables were high- often than expected in cases in which a flock ly correlated (P < 0.001). Thus, we reduced the was observed to contain more than one individ- number of variables included in the analyses to ual (sign test P < 0.05). tree height, percent canopy cover, basal area of We recorded an average of 23.4 -C-2.0 for- and deciduous trees to avoid colinearity of aging maneuvers for 12 species (Table 2). Bird variables. The first two rotated factors from the MIXED-SPECIES BIRD FLOCKS IN MIDDLE AMERICA 669

$ 2.0 of Middle and South American mixed-species = Slate-throated Redstart flocks (lo-48 species;Powell 1985). Fewer spe- 1.5 -. Red-faced Warbler cies in pine and pine-oak dominated forest .‘ Crescent-chested flocks may reflect the simpler habitat structure 2 1.0- Warbler I Hetit or increased latitude of these sites relative to Warbler moist tropical forests where most research on 3 TOVUlSenUS ” 0.5 - Blackthroated - Warbler mixed species flocks has been conducted. . Green Warbler. 0” . Olive Warble Other studies have cited the restriction of 3 0.0 - . Wilsons’ Warbler flock activities to a discrete home range, and our . Golden-&eked Warbler is estimates of home range sizes fall within the 9 -0.5 - range described in other studies of mixed-spe- 0 Bla&-and-&Me‘ Warbler - Graces’ Warbler. cies foraging flocks in the Neotropics (0X-14.3 ha) (Buskirk et al. 1972, Munn and Terborgh .Blue-be~edVlm ; j $ ;;#I1 ; ; 1979, Jullien and Thiollay 1998). Furthermore,

-3 -2 -1 0 1 2 other accounts report that flocks make pre-dusk movements toward water to bathe (Munn and More Open/Coniferous/Shorter Terborgh 1979, Powell 1979) and do not appear to roost together at night (Davis 1946, Buskirk FIGURE 1. Principlecomponents ordination of bird speciesoccurring in 2 15% of flocks,and Red-faced et al. 1972, Munn and Terborgh 1979). We did Warbler,and axesderived from habitatvariables mea- not observe vigorous chasesor supplantings be- suredat randompoints on 42 I-km transects,1995- tween members of different flocks at flock home 1998. range boundaries (Jones 1977, Munn and Ter- borgh 1979, Gradwohl and Greenberg 1980), al- though we did observe increased amounts of vo- principal components analysis accounted for calization when different flocks came into con- 88% of the variability in abundance of bird spe- tact that might be associatedwith inter-flock ag- cies among transects.There was substantial var- gression (Buskirk et al. 1972). iability among species in patterns of vegetation use (Fig. 1). Townsend’s Warblers were most POTENTIAL COSTS OF FLOCKING abundant on transects with moderately closed, Flock attendance might involve a cost in terms moderately tall-stature mixed forest, Hermit, of foraging efficiency if birds have to compro- Black-throated Green, Olive, and Grace’s War- mise their optimal foraging speed to match the blers were most abundant on transectswith short speed of the flock (Jones 1977, Hutto 1988) or to medium-stature, open-canopy pine forest, if their territory boundaries do not coincide with Slate-throated Redstarts, Red-faced and Cres- the territory boundaries of the flock (Munn and cent-chested Warblers were most abundant on Terborgh 1979, Powell 1979). We do not have transectswith relatively open, tall, mostly decid- information on species-specific flock participa- uous forest, and Golden-cheeked, Wilson’s and tion in relation to hock speed; however, if cer- Black-and-white Warblers, and Blue-headed tain species were associated with slow flocks Vireos used mixed forest of intermediate char- and others with fast-moving flocks, we would acteristics. expect to see negative correlations between spe- cies characteristic of slow versus fast-moving DISCUSSION flocks. In contrast to this prediction, we ob- FLOCK STRUCTURE AND DYNAMICS served far fewer negative correlations among The size of our flocks falls within the range of species than expected by chance. Similarly, we 640 individuals typical of Middle and South found little evidence to supportthe assertionthat American mixed-species flocks (Powell 1985). the occurrence of some species is limited to The number of species we found per flock is flocks whose territories coincide with their ter- similar to those reported by Latta and Wunderle ritories because few species occurred out of (1996) in pine forests on Hispaniola (7 species), hocks. and Hutto (1987) and Gram (1998) in Mexican An additional cost of flock attendance could pine-oak forests (18.3 and 9.93 species, respec- be increased competition for food, a factor tively), which is low compared to most studies which could potentially restrict the participation 670 DAVID I. KING AND JOHN H. RAPPOLE in flocks by specieswhich use similar resources would predict that speciesthat are positively as- (Jones 1977, Munn and Terborgh 1979, Hutto sociated among flocks would exhibit similar for- 1988). However, the vast majority (94%) of sig- aging behavior (Hutto 1994). In contrast to this nificant correlations among species occurrences prediction, we only observed one case in which in our flocks were positive, and the foraging be- a species pair (Wilson’s Warbler and Slate- havior of two of the three speciespairs that were throated Redstart) was both positively correlated negatively correlated, and for which we have in flocks and exhibited similar patterns of for- foraging data (Tufted Flycatcher and Black- aging behavior. Conversely, species pairs that throated Green Warbler, Common Bush-Tanager exhibited similar foraging behavior (Slate- and Greater Pewee) were dissimilar. Tufted Fly- throated Redstart and Red-faced Warbler, catchers (n = 9) foraged entirely on airborne Grace’s and Olive Warbler) were not positively prey, whereas Black-throated Green Warblers correlated in flocks. Finally, the flocks we ob- only took 11% of airborne prey (unpubl. data). served occupied relatively small home ranges Similarly, Common Bush-Tanagers (n = 6) for- and traversed them regularly, and therefore, aged entirely on prey on vegetation, whereas probably had a substantial amount of familiarity Greater Pewees (n = 6) foraged entirely on air- with the location of food resources that would borne prey. Thus, it appears that if competition decrease the importance of information gained exists among speciesfor food, it is not mitigated from flock mates (Moynihan 1962, Powell by selective avoidance by speciesof flocks con- 1985). taining potential competitors (Hutto 1994). It is Mutual association with vegetation character- possible that the differences in foraging behavior istics. An alternative explanation for the prepon- we observed among species within flocks is a derance of positive correlations among bird spe- form of characterdisplacement, which could ex- cies pairs in flocks considered by Hutto (1994) plain the lack of evidence of exclusion of spe- and Latta and Wunderle (1996) is that positive cies from flocks by competing species (Jones correlations among species result from similar 1977). However, if this were the case, we would association with particular vegetation character- expect to observe negative correlations among istics. Our observation that Slate-throated Red- species with similar foraging behavior, a pattern starts,Crescent-chested Warblers, and Red-faced that was not apparent in our study. Warblers were positively associated in flocks and also similar to each other in vegetation use RELATIONSHIPS AMONG SPECIES provides some support for this explanation. Foraging enhancement. Flocking behavior may However, other speciesthat were similar in veg- confer advantages to flock members by enhanc- etation use (Black-throated Green, Olive, and ing foraging efficiency. For instance, birds may Hermit Warblers) were not positively associated benefit from the presence of flock mates who within flocks. Furthermore, Townsend’s War- flush concealed prey (Moynihan 1962, Munn blers were consistently associatedin flocks with and Terborgh 1979, King and Rappole, in press). Blue-headed Vireos, Hermit Warblers, Black- Although we did not observe any casesin which and-white Warblers, Slate-throated Redstarts, a bird captured a prey item flushed by another Golden-cheeked Warblers, Crescent-chested bird during our study, flocking birds could cause Warblers, and Red-faced Warblers, but do not subtle evasive movements by prey that might be exhibit close similarities with any of these spe- sufficient to reveal the prey items to foraging cies in terms of vegetation use. birds yet still be beyond the ability of human Anti-predator benejits. Although the potential observers to detect (Powell 1985). Thus we are for flocking to decreasethe vulnerability of flock unable to rule out the potential importance of the members to predation is widely cited (Hutto “beater effect” to flock members. 1988, Thiollay and Jullien 1998) previous dis- Flock members also could benefit from flock cussions have dismissed predation as an impor- mates by using information to exploit patchily tant influence on the species composition of distributed resources (Ward and Zahavi 1973), flocks, maintaining that information about ap- or by copying modes of exploitation of certain proaching predators is transmitted by auditory food items or microhabitats (Valburg 1992). cues, and therefore, flock mates are equally suit- However, if flock members benefited from able as sentinels regardlessof where they forage shared information about food resources, we within the flock (Hutto 1994, Latta and Wun- MIXED-SPECIES BIRD FLOCKS IN MIDDLE AMERICA 671 derle 1996). However, Davis (1975) found that ACKNOWLEDGMENTS alarm signals in pigeons (Columba Zivia) could We thank S. Thorn for her invaluable assistancein be transmitted by subtle behavioral cues that coordinatingthe field work in Honduras.The U.S. Fish would presumably be more easily detected at and Wildlife Service, Region II, provided funding for close proximity. Furthermore, flock mates also the work, and we thank Carol Beardmore and Kathy decrease the probability of an individual being Granillo for their assistancein arranging for this sup- port. Hewlett-Packard Corporation donated the com- selected as prey during an attack on the flock, a puter facilities. W. Barrow, J. Diez, T Holt, 0. Iglesias, benefit that should also be best realized when J. Leiba, M. Martinez, D. Menendez, J. Milam, J. Mi- flock mates are in close proximity (Hamilton guel Ponciano, and J. Vega Rivera provided field as- 1971, Vine 1971). sistance.We also received cooperationfrom the Hon- duran Forestry Department (COHDEFOR), for which If birds benefit from associating with flocks we are extremelv grateful. We thank L. Villela of BIO- because other flock members serve as sentinels CONSULT for &&iding valuable information on Cus- or alternative targets to predators, and if this uco Park to us, and Fundaci6nPastor Fasquelle for use benefit is greater for birds that forage in close of the facilities at Cusuco Park. J. E Hemandez Es- proximity to each other, then it follows that con- cobar coordinatedour Guatemalavisit. J. Morales Can of CONAP (Consejo National de Areas Protegidas) specifics would be the most likely candidates, provided permits for our Guatemala work. A. Dix, 0. since they are most similar in foraging behavior. Nunez, I. de la Rota, 0. Rojas, and C. Castaneda,all However, conspecificsalso would compete most of Fundaci6n Defensores de la Naturaleza, provided closely for resources.These suggestionslead to information and accessto field sites. Herman Kihn of Centro de Datos para la Conservaci6n (CDCCECON) some interesting predictions. First, flock mem- gave helpful advice on specific goldencheeklocalities. bers should exhibit territoriality towards other W. Barrow of the U.S. Geological Survey’s Biological conspecifics because they are least able to re- ResourcesDivision provided project oversight and co- duce competition through character displace- ordination, as well as assistancewith field work. J. L. ment (Jones 1977). Second, in instances where Rangel, M. A. Castillo, M. A. Vazquez, and I. March Mifsut, all of El Colegio de la Frontera Sur (ECO- a conspecific flock member is tolerated, the two SUR), provided critical information and assistancefor should be of different sexes, because this will our work in Mexico. Martin R. Gonzalez Hemandez, maximize the potential for partitioning resources El Delegado Federal, ProcuraduraFederal de Protec- through intersexual differences in foraging. Our cion al Ambiente, Delegation Chiapas, SEMARNAP provided Mexican permits with assistancefrom An- observation that most bird species in our study gelica Narvaez of the U.S. Embassy in Mexico City. were represented within flocks by a single in- dividuals more often than expected, and that in LITERATURE CITED cases in which a flock was observed to contain BUSKIRK,W. H., G. V. N. POWELL,J. E WIT~ENBERGER, more than one individual, the species was rep- R. E. BUSKIRK,AND T U. POWELL.1972. Interspe- resented by members of both sexes more often cific bird flocks in tropical highland Panama.Auk than expected, are consistent with these predic- 89:612-624. tions. Although we observed no sex-specificdif- DAVIS, D. D. 1946. A seasonal analysis of mixed ferences in foraging behavior between male and flocks of birds in Brazil. Ecology 27:168-181. DAVIS,J. M. 1975. Socially induced flight reactionsin female Black-and-white or Golden-cheeked the pigeon. Anim. Behav. 23597-601. Warblers, males of both of these speciesforaged ELGAR,M. A. 1989. Predator vigilance and group size higher than females, although this difference in mammals and birds: a critical review of the was significant only for Golden-cheeked War- empirical evidence. Biol. Rev. 64: 13-33. GRADWOHL,J., AND R. GREENBERG.1980. The forma- blers (tz8 = 2.13, P = 0.04). Others have ob- tion of antwren flocks on Barro Colorado Island, served the co-occurrence in flocks of members Panama. Auk 97:385-395. of the opposite sex for transient or wintering mi- GRAM, W. K. 1998. Winter participation by Neotropi- grants (Zahavi 1971, Leek 1972, Gradwohl and cal migrant and resident birds in mixed-species Greenberg 1980). Because it is extremely un- flocks in northeasternMexico. Condor 100:44-53. HAMILTON,W. D. 1971. Geometry for the selfish herd. likely that any reproductive factors are involved J. theor. Biol. 31:295-311. in these occurrences,the best explanation would HEJL, S. J., J. VERNER,AND G. W. BELL. 1990. Se- seem to be that birds are exploiting conspecifics quential versus initial observations in studies of for protection from predators while minimizing &ian foraging. Stud. Avian Biol. 13:166-173. HOWELL,N. G., AND S. WEBB. 1995. A guide to the the costs of competition for food by preferen- birds of Mexico and northern Central America. tially flocking with conspecifics of slightly var- Oxford Univ. Press, New York. iant foraging behavior and/or morphology. Hurro, R. L. 1987. A description of mixed-species 672 DAVID I. KING AND JOHN H. RAPPOLE

insectivorousbird flocks in western Mexico. Con- MOYNIHAN,M. 1962. The organization and probable dor 89:282-292. evolution of some mixed species flocks of Neo- HUGO, R. L. 1988. Foraging behavior patternssuggest tropical birds. Smithson. Misc. Coll. 143:l-140. a possible cost associated with participation in MUNN, C. A., AND J. W. TERBORGH.1979. Multi-spe- mixed-speciesbird flocks. Oikos 51:79-83. ties territoriality in Neotropical foraging flocks. HUTTO,R. L. 1994. The composition and social orga- Condor 81:338-347. nization of mixed-species flocks in a tropical de- POWELL,G. V. N. 1979. Structure and dynamics of ciduous forest in western Mexico. Condor 96: interspecific flocks in a Neotropical mid-elevation 105-l 18. forest. Auk 96:375-390. JAMES,I? C., AND H. H. SHUGART.1970. A quantitative POWELL,G. V. N. 1985. Sociobiology and adaptive sig- method of habitat description. Am. Birds 24:721- nificance of interspecific foraging flocks in the -736 Neotropics. Ornithol. Monogr. 36:713-372. I _I”. JONES,S. E. 1977. Coexistence in mixed species ant- PULLIAM,H. R. 1973. On the advantagesof flocking. wren flocks. Oikos 29:366-375. J. theor. Biol. 38:419-422. JULLIEN,M., ANDJ. THIOLLAY.1998. Multi-species ter- SOKAL,R. R., AND E J. ROHLF.1995. Biometry. 3rd ritoriality and dynamic of Neotropical forest un- ed. W. H. Freeman., New York. derstory bird flocks. J. Anim. Ecol. 227-252. SULLIVAN,K. A. 1984. The advantagesof social for- aging in downy woodpeckers. Anim. Behav. 32: KING, D. I., AND J. H. RAPPOLE.In press. Commensal 1, *n foraging relationships of the White-browed Fan- IO-U. tail (Rhipidurn aureola) in Burma (Myanmar). J. THIOLLAY,J., AND M. JULLIEN.1998. Flocking behavior Bombay Nat. Hist. Sot. of foraging birds in a Neotropical rain forest and the antipredatordefense hypothesis. Ibis 140:182- LATTA, S. C., AND J. M. WUNDERLE.1996. The com- position and foraging ecology of mixed-species 194. VALBURG,L. K. 1992. Flocking and frugivory: the ef- flocks in pine forests of Hispaniola. Condor 98: fect of social groupings on resource use in the 595-607. Common Bush-Tanager.Condor 94:358-363. LECK,C. E 1972. The impact of some North American VINE, I. 1971. Risk of visual detection and pursuit by migrants at fruiting trees in Panama.Auk 89:842- a predator and the selective advantageof flocking 850. behavior. J. theor. Biol. 30:405-422. MILLER,R. C. 1922. The significanceof the gregarious WAGNER,J. L. 1981. Visibility and bias in avian for- habit. Ecology 3:122-126. aging data. Condor 83:263-264. MORRISON,M. L. 1984. Influence of sample size and WARD, P, AND A. ZAHAVI. 1973. The importance of sampling design on analysis of avian foraging be- certain assemblagesof birds as “information cen- havior. Condor 86:146-150. ters” for finding-food. Ibis 115:517-534. MORSE,D. H. 1970. Ecological aspectsof some mixed- ZAHAVI. A. 1971. The social behavior of the White speciesforaging flocks of birds. Ecol. Monogr. 40: Wagtail (MotucilZu alba) wintering in Israel. Ibis 168-199. 113:203-211.