The Condor90~761-772 0 The Cooper Ornithological Society 1988
BIRD ABUNDANCE AND SEASONALITY IN A COSTA RICAN LOWLAND FOREST CANOPY’
BETTE A. LOISELLE~ Department of Zoology, Universityof Wisconsin,Madison, WI 53706
Abstract. I censusedforest canopy birds from two emergent trees in lowland wet forest in Costa Rica from April 1985 to May 1986. Composition of the canopy avifauna did not differ overall between censussites. I recorded 89 speciesand 2,944 individuals during 49 censuses.Forest canopy was dominated by frugivores, especially large-bodied (> 100 g) frugivores,and parrots.Furthermore, in contrastto the avifauna of forestcanopies in Panama and Peru, I found that the canopy avifauna was primarily composedof forest species,rather than scrub species.Most speciesoccurred in intra- or interspecific flocks. I found that the abundance of small frugivores and small insectivores was seasonallyvariable. Extent of seasonalvariation in fruit crop sizes of Dipteryx panamensismay have contributed to the annual variation observedin psittacids.Avifauna of the forest canopy, with few exceptions, was distinct from the understory avifauna; few of the common understory specieswere recordedin the canopy. Further, in contrastto the canopy avifauna, the understoryavifauna was dominated, in terms of speciesnumber, by insectivores. Key words: Canopy; CostaRica; frugivores;rain forest;seasonality; tropical.
INTRODUCTION and leaf loss than understory trees and shrubs Bird species that live in neotropical forest can- (Opler et al. 1980). Canopy habitats have more opies comprise 40 to 50% of forest bird species seasonal populations of insects than do under- (Stiles 1983; Blake et al., in press; Karr et al., in story habitats (Fogden 1972, Smythe 1982). For press). Canopy trees provide leaf, flower, and these environmental and biotic reasons, birds of fruit resources for birds and other organisms. the forest canopy are predicted to be more vari- Despite the clear importance of the canopy to an able seasonally than understory birds (Pearson understanding of tropical forest communities, 1971, Karr 1976). little work has been completed on birds in this To test the prediction of greater seasonality in canopy bird assemblages, I censused birds from forest zone (but see Pearson 197 1, Lovejoy 1974, Greenberg 198 1, Munn 1985). Instead, many two emergent canopy trees in lowland wet forest studies have focussed on birds inhabiting the for- of Costa Rica. This canopy study is the first that est understory (e.g., Munn and Terborgh 1979; reports results from more than one location in a Gradwohl and Greenberg 1980; Karr 1980; Karr forest canopy. Furthermore, because this Costa and Freemark 1983; Levey 1986; Wong 1986; Rican forest is less seasonal and wetter than the forest censused in Panama (Greenberg 198 l), it Loiselle and Blake, in press). Canopy and understory habitats are markedly provides a good comparison to evaluate the de- different in tropical lowland wet forests. The can- gree of seasonality of birds in the Costa Rican opy is subject to greater daily variation in light, canopy relative to the Panamanian forest cano- temperature, wind, and rainfall than is the buff- py. I evaluate seasonality of canopy birds, vari- ered, dark forest understory (Allee 1926, Fetcher ability between census trees, and compare those et al. 1985). In Costa Rican wet forest, the site canopy results with ongoing bird studies of the of this study, fruiting and flowering peaks also understory avifauna. differ between canopy and understory trees METHODS (Frankie et al. 1974). Furthermore, canopy trees I conducted canopy censuses in lowland wet for- show greater seasonality of flowering, fruiting, est at Estacion Biologica La Selva (10”25’N, 84”O 1‘W), Costa Rica (for detailed description of I Received 16 November 1987. Final acceptance6 this site see Hartshorn 1983). La Selva receives May 1988. 2 Present adddress:Natural ResourcesResearch In- about 4 m of rain annually (Organization for stitute, 3151 Miller Trunk Highway, University of Tropical Studies, unpubl. rainfall data). During Minnesota-Duluth, Duluth, MN 558 11. the course of this study, rainfall at La Selva was
[7611 162 BETTE A. LOISELLE
TABLE 1. Distributionof canopycensuses by season Socrates durissima, Apeiba membranacea, and from Tree 1 and Tree 2. LD, LW, ED, and EW rep- Pentaclethra macroloba. Some major vines in- resent late dry (March-April), late wet (September- cluded Norantea sessilis,Souroubea sp., and Clu- November), early dry (late December-February), and early wet (May-August) seasons,respectively. sia sp. In contrast, Hymenolobium was located along the major ridge that divides the main pri-
LD 85 EW 85 LW 85 ED 86 LD 86 mary forest block of La Selva (“old” La Selva). Some major trees near this census site included Tree 1 3 8 7 5 Tree 2 1 2 5 z 5 Virola koschnyi, Pentaclethra macroloba, Mi- conia multispicata,Socrates durissima, and Wel- jiu georgii. An unindentilied vine in the Rubi- aceae covered much of the surrounding foliage. below normal (total rainfall = 2,847 mm). To I conducted 49 censusesfrom 1 April 1985 to facilitate seasonal comparisons of the canopy 28 April 1986 (Table 1). Censusesbegan at sun- avifauna, I divided the year into four periods, rise (about 06:OO). The Dipteryx (hereafter re- early and late dry, and early and late wet seasons ferred to as Tree 1) supported a platform 32 m (Table 1). I selected these periods on the basis above the ground and I was able to conduct 30 of rainfall totals before examining bird census 3-hr censusesfrom this tree. I restricted my cen- data. Becauseplant phenology is strongly influ- susto 2 hr while in the Hymenolobium (hereafter enced by rainfall (e.g., Frankie et al. 1974), these referred to as Tree 2) (19 censuses)because no divisions also indirectly reflect plant phenolog- platform was available and I had to conduct the ical patterns. censuswhile hanging from the rope at 30 m. The I used climbing ropes (Perry 1978) to gain first censusconducted from this tree lasted only access to the canopies of two emergent trees 1 hr and was not included in statistical testscom- (Dipteryx panamensis and Hymenolobium pul- paring results from the two trees. cherrimum), each located more than 500 m from All birds seenor heard within 100-l 25 m were the forest edge. I selectedthe two trees because recorded in 15-min intervals. The maximum their height and emergence above most trees of number of individuals per speciesrecorded dur- the canopy permitted greater visibility. Dipteryx ing any 15-min period was used for analysis of has been the site of previous canopy studies at census results (see Loiselle 1987a). I measured La Selva (e.g., Perry and Starrett 1980, Fetcher distances to nearby canopy trees with a range- et al. 1985) and is located near a permanent finder during the first few censuses.These dis- stream (Quebrada El Salto). Major tree species tances were then used to estimate distances to visible from this tree and within the censusarea birds recorded during these and later censuses. (approximately 3.5 ha) included Dipteryx pan- The direction in which a recorded bird was seen amensis,Mnquartia guianensis,Lecythis ampla, or heard was noted to avoid double counting
TABLE 2. Mean number (SE) of individuals and speciesseen per censusduring five seasonsin 1985-1986 from Tree 1 (1) and Tree 2 (2). Seasonsare identified in Table 1. Mean values are given for both entire census period (3 hr) and the first 2 hr only from Tree 1. These latter values are directly comparable to those reported from Tree 2 and were used for statisticaltests.
Latedry 1985 Early wet 1985 Late wet 1985 Early dry 1986 1 2 I 2 I 2 1 2
A. Tree 1 (all birds) Individuals 82.0 - 48.6 - 62.1 - 63.7 - (1.53) - (5.00) - (3.83) - (3.00) - Species 26.0 - 22.1 - 29.0 - 33.0 - (2.00) - (1.71) - (1.23) - (0.50) - B. Tree 1 and Tree 2 (equal censuslength) Individuals 74.7 - 39.8 44.0 51.1 62.6 54.6 58.2 (3.33) - (4.54) (11.0) (4.13) (7.49) (3.93) (2.86) Species 22.7 - 19.0 17.0 24.4 28.4 28.9 31.3 (0.88) - (1.80) (2.00) (1.46) (2.29) (1.08) (1.14)
aMeans not reported because census length was less than 2 hr. SEASONALITY IN CANOPY BIRDS 763 within each 15min period. Birds flying by or over the canopy were not recorded unless they landed in the census area. Activity declined markedly after OS:00 and few individuals or specieswere added in the third hour. However, to compare abundances in the two trees, I did not include new individuals or speciesthat were recorded in the third hour from Tree 1. I divided canopy birds into nine major guilds based on size and diet to evaluate seasonal changesin abundance of birds in relation to their primary resources. These guilds were small- >0-0.5 >0.5-1.0 >i.O-2.0 >2.0-3.0 > 3.0 (< 100 g) and large-bodied (> 100 g) frugivores, AVE. NO. INDIVIDUALS/CENSUS seedpredators (parrots), small- and large-bodied FIGURE 1. Frequency histogram showing percent- insectivores, nectarivores, frugivore-nectari- age of specieswith number of individuals per census vore-insectivores, raptors, and scavengers (see as indicated. Appendix). Both small- and large-bodied frugi- vores also take insects, and some (e.g., Ram- phastos)take lizards and frogs(Skutch 1972). My divisions are broad and that some speciescould goal was to distinguish birds that regularly eat be further separatedby finer subdivision. How- fruit from birds that rely almost entirely on in- ever, broad categoriesare more appropriate for sects.I did not distinguish fruit dispersers(e.g., the sample sizes observed; the frequent absence Ramphastos)from some seedpredators (e.g., Co- of speciesfrom censuses(Fig. 1) indicates that lumba), but I did distinguish parrots as a separate entire guilds could be absent from some censuses guild because their bill morphology results in if subdivisions were finer. little overlap in diet with other fruit and seed I used ANOVA to evaluate differences in the eaters (pers. observ.). Most large-bodied insec- canopy assemblage between trees and among tivores (e.g., Monasa) also take small vertebrates seasons(Sokal and Rohlf 198 1). I used Kruskal- (Skutch 1972; Pearson 1975; Sherry 1983; Stiles Wallis analysis of variance to test for seasonal 1983; pers. observ.). Nectarivores also eat insects differencesamong guilds when normality of data and spiders.I did not separateeither nectarivores setswas violated (Shapiro and Wilk 1965, Sokal or frugivore-nectarivore-insectivores by body and Rohlf 198 1). All other statistical tests are size. Raptors and scavengersaccounted for only identified in the text. English and scientificnames 1.4% of birds seen, and further division of these of all birds seen in the canopy are in the Appen- guilds seemed unwarranted. I realize that these dix and follow AOU (1983, 1985, 1987). RESULTS GENERAL COMPOSITION
TABLE 2. Extended. I recorded a total of 89 species, including 82 speciesfrom Tree 1 and 72 speciesfrom Tree 2
Late dry 1986 All (Appendix). A majority of species (75%) aver- I 2 I 2 aged fewer than one individual per census (Fig. 1). Distribution of speciesamong different abun- dance classes(Fig. 1) did not differ betweeen cen- 68.4 - 61.9 (2.36) - (2.49) 1 sus sites (x2 = 2.64, df = 4, P > 0.60). With all 36.4 - 29.0 censusescombined, however, significantly more (0.51) - (1.10) 1 specieswere seen on average from Tree 2 (28.8 species/census)than from Tree 1 (24.9 species/ 60.2 60.2 52.0 58.4 census) (two-tailed t-test, t = 2.32, P < 0.05, (3.67) (4.22) (2.56) (2.85) Table 2). 30.8 31.0 24.9 28.8 Speciescomposition and abundance patterns (1.46) (1.51) (1.04) (1.32) were similar between the two trees. Of the 20 most common species in each tree, 16 species 764 BETTE A. LOISELLE
TABLE 3. Twenty most common speciesrecorded in order of their abundance from censusesconducted in Tree 1 and Tree 2. * Indicates that this specieswas not recorded in the top 20 from the other tree.
Tree I Tree 2 Species Flock Species Flock
Mealy Parrot Y Mealy Parrot Y White-crowned Parrot Y Chestnut-headedOropendola Y Montezuma Oropendola Y Scarlet-rumped Cacique Y Scarlet-rumped Cacique Y Montezuma Oropendola Y Keel-billed Toucan Y Short-billed Pigeon N Olive-backed Euphonia Y Brown-hooded Parrot* Y Chestnut-mandibled Toucan Y Keel-billed Toucan Y Chestnut-headedOropendola Y Olive-backed Euphonia Y Short-billed Pigeon N Chestnut-mandibled Toucan Y Collared Aracari Y Collared Aracari Y Tropical Gnatcatcher Y White-crowned Parrot Y Masked Tityra* Y Red-lored Parrot Y Rufous Piha N Tropical Gnatcatcher Y Red-lored Parrot Y Crowned Woodnymph* N White-ringed Flycatcher* Y Slate-coloredGrosbeak* N Purple-throated Fruitcrow* Y Black-striped Woodcreeper N” Black-striped Woodcreeper N White-fronted Nunbird Y White-fronted Nunbird Y Slaty-tailed Trogon Na Slaty-tailed Trogon N White-shouldered Tanager* Y Shining Honeycreeper* Y Rufous Piha N”
= Occasionally in mixed-spenes flocks. were sharedbetween the two trees(Table 3). These < 0.001) and individuals (F = 3.94, P = 0.02) 24 species(from the 20 most common speciesat observed,but not between treesfor either species both trees) accounted for 76.5% and 77.6% of all (P > 0.15) or individuals (P = 0.09) (Table 2); individuals recorded from Tree 1 and Tree 2, the tree-season interactive effect was not signif- respectively. icant in either case (P > 0.40) (two-way ANO- Frugivores (including parrots) clearly domi- VA). I observed fewer speciesfrom Tree 2 during nated this canopy avifauna, with 18 (75%) of the early wet season1985 than in other seasons(one- most common speciesrepresenting those guilds way ANOVA, Student-Newman-Keuls [SNK] and only four (17%) representing insectivorous multiple range comparisons, P < 0.05; Table 2) species.Nectarivores and frugivore-nectarivore- (Sokal and Rohlf 198 1). Similarly, early wet had insectivoreseach were representedby one species significantly fewer species than either late wet among the 24 most common species.In addition, 1985 or early and late dry season1986 from Tree the canopy assemblageobserved from these two 1 (one-way ANOVA, SNK multiple range test, trees was dominated by speciesfound primarily P < 0.05) (Table 2). in forest habitats. Nineteen (79%) of these 24 In contrast, I observed more individuals from common species are primarily forest canopy Tree 1 during late dry season 1985 than in any species(based on Stiles’ unpubl. Checklist of La other season (one-way ANOVA, SNK multiple Selva Birds; Blake et al., in press).The remaining range comparisons, P < 0.05) (Table 2). There five species (Chestnut-headed Oropendola, was no significant difference in the number of Montezuma Oropendola, Masked Tityra, White- individuals observed from Tree 2 among sea- ringed Flycatcher,and Shining Honeycreeper)are sons; however, no comparable censuses were more frequently found in forest-edgehabitats. In conducted during late dry season 1985 (Table 2). addition, nine of the 10 most abundant forest- I recordedthe fewestindividuals during early wet canopy birds observed in this study from both seasonfrom both trees (Fig. 2, Table 2). censussites forage most often in intra- or inter- Absence of temperate migrants during early specific flocks (Table 3). wet season accounted only minimally for the lower abundance of canopy birds during this sea- SEASONALITY IN CANOPY AVIFAUNA son (seeLoiselle 1987a) (Fig. 2). Migrants in Cos- I found that significant variation occurredamong ta Rica also include speciesfrom higher eleva- seasonsin both number of species(F = 18.9, P tions that descend to La Selva during their SEASONALITY IN CANOPY BIRDS 765
A. TREE 2 - Total 60 --- Total less migrants
- \‘ “,, II i8- \ 2 _ \ 40- 0 , , 5 lo- 1 o SEED B. TREE 1 --A_/ -z _ I I L 0 i4-
60
FIGURE 2. Mean number of individuals recorded per censusby seasonfrom A. Tree 2 and B. Tree 1. LOi Ei85 LW85 ED86 Lo86 Migrantsinclude both temperateand altitudinal mi- SEASON grants.LD85, EWSS,and LW85 arelate dry, earlywet, and late wet season1985; ED86 and LD86 are early FIGURE 3. Mean number of individuals recorded and late dry season1986. per censusby seasonfor designatedguilds from Tree 1. LFRU and SFRU are large-and small-bodiedfru- givores,SEED are parrots,LINS and SINS are large- and small-bodiedinsectivores, FNI are frugivore-nec- nonbreeding season (altitudinal migrants) (Loi- tarivore-insectivores,NECT are nectarivores,and selle 1987b; Blake et al., in press). Those alti- RAPT are raptors.Seasons are as in Figure 2. tudinal migrants were rare (< 1% of all birds cen- sused) in the canopy and were represented by four species(Yellow-eared Toucanet, Three-wat- Tree 2 (SFRU: K-W H = 6.5, df = 3, P = 0.09; tled Bellbird, Bare-necked Umbrellabird, and SINS: K-W H = 7.6, df = 3, P < 0.06). Olive-striped Flycatcher). Seasonal changes in Parrots showed significant seasonal variation canopy-bird abundances are more clearly under- in abundance from Tree 1 only (K-W H = 11.4, stood when individual guilds are examined. df = 4, P -C 0.05), but showed no seasonalvari- Large-bodied frugivores (LFRU), the most ation when the late dry season of 1985 was ex- abundant guild, showed nearly significant sea- cluded (K-W H = 5.2, df = 3, P > 0.15). Other sonal variation in censusesfrom Tree 1 (Kruskal- guilds contributed less to total canopy avifauna Wallis H = 7.7, df = 4, P = 0.10) but not from and showedlittle seasonalvariation in either tree. Tree 2 (K-W H = 2.6, df = 3, P > 0.45) (Figs. Only raptors, which peaked during early dry sea- 3, 4). Seasonal variation in Tree 1 was due to a son 1986, showed significant seasonalvariation large dry season peak in 1985 and when this atTreel(K-WH=14.6,df=4,P
Greenberg (198 1) reported that the BCI can- opy was dominated by scrub species. Pearson (1975) also reported a predominance of scrub speciesin the Peruvian canopy (annual rainfall 1,523 mm), but noted that scrubbirds only rarely were found in the canopy of wetter forests of Ecuador (2,987 mm rainfall annually) and Bo- livia (1,995 mm rainfall annually). The BCI tower from which Greenberg cen- susedis located in younger and drier forest (70 to 100 years old, 2,600 mm/year) than the La Selva and Ecuador forestsand those factors may have accounted for some of the differences ob- served in canopy composition (see Loiselle 1987a). Furthermore, althoughapproximately the same size as La Selva, BCI (1,500 ha) is an island and has lost an estimated 50 forest speciessince
EW.85 LW.85 ED86 Lb86 its isolation (Karr 198213).La Selva, on the other SEASON hand, is connected to foothill and montane for- ests of Parque National Braulio Carrillo. Willis FIGURE 4. Mean number of individuals recorded per censusby seasonfor designatedguilds from Tree (1979) in a study of Brazilian woodlots, found 2. Guild abbreviationsare as in Figure 3. that large canopy frugivores were replaced by edge-living omnivores in small woodlots(see also tarivores); he recorded only three insectivorous Blake 1983; Blake and Karr 1984; Lovejoy et al. species among his 20 most common species. 1986; Levey and Stiles, in press).Thus, the lower Similarly, frugivores dominated the canopy of number ofedge speciesI observedin the La Selva a Peruvian dry forest (Pearson 1971); 83% of forest canopy may reflect the fact that this forest speciesthat spent more than 50% of their for- has not been completely isolated. aging time in the upper strata of this forest were Although I observedseasonality in some guilds fi-ugivores. and overall in the La Selva canopy, the degree Although frugivores dominated the avifauna of seasonalitywas lessthan that reported for BCI in both La Selva and BCI, there were consider- (Greenberg 1981). Higher seasonality at BCI able differences in the species composition of probably was due in large part to the higher abun- common birds. Following Greenberg (198 l), I dance of temperate migrants, particularly Bay- excluded parrots, toucans, pigeons, and cracids, breasted Warblers, in the BCI canopy (Loiselle and reexamined the 20 most common species 1987a). from my two censussites. Only five specieswere among the 20 most common at both BCI and at RESOURCE ABUNDANCE AND La Selva (Tropical Gnatcatcher, Shining Hon- SEASONALITY eycreeper, Squirrel Cuckoo, White-ringed Fly- In general,one might expectthat seasonalchanges catcher,and White-shouldered Tanager). Two of in avian guilds should reflect patterns of resource the four most common speciesat La Selva are abundance(Stiles 1980, 1985; Wheelwright 1983; not present on BCI (Scarlet-rumped Cacique, Martin and Karr 1986). Abundance of small fru- Chestnut-headed Oropendola), but are present givores did, in fact, peak during the period of on the adjacent Panama mainland (Ridgely 1976, peak fruit abundance (late wet season)at La Selva Willis and Eisenmann 1979). In contrast,the four (Frankie et al. 1974). Abundance of large frugi- most common BCI species (Blue Dacnis, Bay- vores, however, did not peak during this period. breasted Warbler, Lesser Greenlet, and Plain- The influence of a major fruit crop to bird abun- colored Tanager) were recorded from the La Sel- dance is illustrated by Tree 1 (D. panamensis). va canopy, but in low numbers. These species Parrots often fed heavily on fruits of Dipteryx are more common in secondgrowth and forest- trees, which normally fruit from November to edge habitats at La Selva (Stiles, unpubl. Check- March (Frankie et al. 1974). During late dry sea- list of La Selva Birds). son 1985, Dipteryx crops were large and many SEASONALITY IN CANOPY BIRDS 767
White-crowned Parrots were foraging in the cen- species,as well as occurrenceof rare species,will sus tree and in nearby Dipteryx trees (Fig. 3). In vary among years. For example, Great Green contrast, the Dipteryx crop in the censustree was Macaws (ha ambigua) were relatively common not as large during dry season 1986 as in 1985 at La Selva from November 1986 to April 1987 (pers. observ.) and fewer parrots were present. and undoubtedly would have been recorded in Abundance of small insectivores also appeared canopy censusesconducted during this period. to be related to resourcelevels; their abundance Macaws typically were observed feeding on fruit- was highest during periods of leaf flushing (late ing Dipteryx trees and their irregular occurrence dry-early wet season), a period of high insect at La Selva may reflect spatial and temporal vari- abundance (Fogden 1972; Wolda 1978, 1982) ation in fruit crops, as well as effectsof human- and insect activity (Janzen 1983). Moreover, sea- caused disturbance (e.g., logging). sonality of insects is most pronounced for those Long-term changesin the La Selva avifauna from the 5-15 mm size class (Smythe 1982), also are likely to influence the composition of the range taken most frequently by small insec- canopy birds. During the past 30 years, more tivores (Hespenheide 197 1, Karr 1976, Smythe canopy speciesat La Selva have declined than 1982). Large-bodied insectivores,in contrast,did any other group (Levey and Stiles, in press).Doc- not show any significant seasonal pattern of umenting both annual and seasonalfluctuations abundance. Lack of seasonal variation in large in forest-canopy birds may increase our under- insectivoresmay reflect lower seasonalityoftheir standing of the causesand consequencesof long- large insect prey or the fact that many large in- term changesin this group (Karr 1982a). sectivores also often feed on alternative prey, such as small vertebrates. Thus, resource avail- COMPARISON WITH UNDERSTORY ability likely influences seasonal variability of AVIFAUNA some birds observed in these censuses. I sampled forest understory birds at La Selva Nectarivores, becauseof their small size, often with mist nets during the same period as I con- were difficult to observe in the canopy and their ducted canopy censuses(Loiselle 1987b). Dis- abundance likely was underestimated relative to tribution of captures of understory birds (Fig. 5) other guilds. Nectarivores were observed more approximated the result presented for canopy often from Tree 1 during the early wet season birds (Fig. 1) (Chi-Square testof number of species (Fig. 3) a period of high flower availability at La in each abundance category: x2 = 5.9, df = 8, P Selva (Frankie et al. 1974) but were more com- > 0.60). This pattern, many rare speciesand few mon at Tree 2 during late wet season(Fig. 4), a common ones, also has been observed in other period of low flower availability. Low numbers tropical studies (e.g., Karr et al., in press). of observations in both trees (usually less than Despite different techniques employed in cen- three individuals per census) may obscure sea- susing birds of these two strata, I believe the 20 sonal patterns. most common speciescaptured in mist nets (Ta- F. G. Stiles (pers. comm.) also has noted con- ble 4) adequately representthe common birds of siderable variation in daily and weekly abun- the forest understory. Abundance of large, dance of canopy birds that appear tied to re- ground-dwelling birds, such as tinamous, cur- sources.For example, when flowering, Norantea, assows,and quail-doves are underestimated by a canopy vine, attracted large numbers of tem- mist nets, but form a small proportion of the perate migrants (F. G. Stiles, pers. comm.). avifauna, based on visual/auditory observations. Unlike the frugivore-dominated canopy, insec- ANNUAL VARIATION IN CANOPY tivores accounted for the greatest number of AVIFAUNAS speciesin the forest understory (Table 4) (seealso Short-term studies in the tropics provide useful Levey 1986; Blake et al., in press). However, in information but must be interpreted cautiously terms of number of individuals captured, under- (Wiens 1977; Stiles 1978, 1983; Wolda 1978; story frugivores were as abundant as insectivores Foster 1982; Wheelwright 1986; Levey 1987). (Loiselle 1987b). A similar pattern has been not- My results suggestthat identities of the common ed elsewhere by Stiles (1983, for La Selva), core of the canopy avifauna observed here likely Greenberg (1981, for BCI), and Karr (1976, for will remain similar from year to year. However, Panama mainland). I further found that for seasonal patterns in abundance of common understory populations, insectivore capture rates 168 BETTE A. LOISELLE
TABLE 4. Twenty most common species(in decreas- ing order of mist-net captures)in the forest understory at La Selva (Loiselle 1987b). * indicates that these speciesalso were observed in the forest canopy. N = nectarivore, I = insectivore, F = frugivore.
Species Gudd
*Wedge-billed Woodcreeper Glyphorynchusspirurus I *Red-capped Manakin Pipra mentalis F Ochre-bellied Flycatcher Mionectesoleagineus F/I *Long-tailed Hermit d Phaethornissuperciliosus N A :, :, A A Wood Thrush A 6 z A A Y Hylocichla mustelina I/F CAPTURES/ SAMPLE White-ruffed Manakin Corapipo leucorrhoa F FIGURE 5. Frequency histogram showing percent- Bicolored Antbird age of specieswith number of individuals captured in Gymnopithysleucaspis I forest understory per sample as indicated (from Loi- White-breasted Wood-Wren selle 1987b). Henicorhina leucosticta I Ocellated Antbird Phaenostictusmcleannani I Spotted Antbird these species (Crowned Woodnymph and Tawny- Hylophylax naevioides I crested Tanager) regularly. Stiles (1980) noted Plain-brown Woodcreeper that male and female Crowned Woodnymphs Dendrocinclajiiliginosa I Bronze-tailed Plumeleteer differed in vertical foraging preferences with males Chalybura urochtysia N occurring more often in the canopy than females. Olive Tanager Both Stiles (1983) and Pearson (1971, 1977) ob- Chlorothraupiscarmioli F/I served that canopy birds foraged over a greater Swainson’s Thrush Catharus ustulatus F/I vertical range compared to understory birds. Ruddy-tailed Flycatcher Terenotriccuserythrurus I CONCLUSIONS *“Tawny-crested Tanager Frugivores (> 100 g) and parrots dominated the F/I Tachyphonusdelatrii canopy at La Selva. I observed significant sea- Song Wren Cyphorhinusphaeocephalus I sonal variation among some guilds and the can- bBlack-facedAntthrush opy assemblage as a whole, but seasonality of Formicarius analis I this assemblage appeared less than that observed *“Crowned Woodnymph in Panama by Greenberg (198 1). Results from a Thalurania colombica N single-year study of La Selva canopy birds con- Tawny-crowned Greenlet Hylophilus ochraceiceps I ducted from only two sites should be interpreted cautiously. More long-term studies on canopy a,bRepresent species with equal number of captures assemblages with simultaneous monitoring of re- sources are needed. as a whole displayed less seasonality than either ACKNOWLEDGMENTS understory frugivores or nectarivores (Loiselle 1987b), a pattern that also was apparent in the J. G. Blake, R. L. Hutto, J. F. Kitchell, D. J. Levey, canopy censuses and elsewhere (Karr 1976, Mar- T. E. Martin, T. C. Moermond, K. Rusterholz, F. G. Stiles, and D. M. Waller provided helpful comments tin and Karr 1986). Unfortunately, because of on earlier drafts of this paper. I thank Manuel Santana the different sampling techniques, I am not able for his help and advice in placingcanopy ropes. I thank to directly compare the degree of seasonal vari- D. A. and D. B. Clark for their logistical support and ation of guilds between canopy and understory encouragementat La Selva. The following agencies provided supportfor this study:Noyes Fellowship (Or- habitats. ganization for Tropical Studies), Joseph Henry Fund Five common understory birds were observed (National Academy of Sciences),Stewart Award (Wil- in the canopy (Table 4) but I saw only two of son Ornithological Society), Ibero-American Studies SEASONALITY IN CANOPY BIRDS 169
Grant, and University of Wisconsin (Department of KARR, J. R. 1976. Seasonality,resource availability, Zoology). and community diversity in tropical bird com- munities. Am. Nat. 110:973-994. LITERATURE CITED KARR, J. R. 1980. Geographicalvariation in the avi- faunasof tropical forestundergrowth. Auk 97:283- ALLEE,W. C. 1926. Measurement of environmental 298. - factorsin the tropical rain-forest of Panama. Ecol- KARR, J. R. 1982a. Population variability and ex- ogy 7:273-302. tinction in the avifauna of a tropical land bridge AMERICANORNITHOLOGISTS UNION.’ 1983. Check- island. Ecology 63:1975-1978. list of North American birds. 6th ed. American KARR. J. R. 1982b. Avian extinctions on Barro Col- Ornithologists’ Union, Washington, DC. orado Island, Panama: a reassessment.Am. Nat. AMERICANORNITHOLOGISTS UNION.’ 1985. Thirty- 119:220-239. fifth supplement to the American Ornithologists’ KARR, J. R., AND K. FREEMARK. 1983. Habitat se- Union Check-list of North American birds. Auk lection and environmental gradients:dynamics in 102:680-686. the “stable” tropics. Ecology 64: 1481-1494. AMERICANORNITHOLOGISTS UNION.’ 1987. Thirty- KARR, J. R., S. K. ROBINSON,J. G. BLAKE,AND R. 0. sixth supplementto the American Ornithologists’ BIERREGAARD,JR. In press. The avifauna of four Union Check-list of North American birds. Auk neotropical forests. In A. Gentry [ed.], Four neo- 104:591-596. tropical forests: a comparison of La Selva, Costa BLAKE,J. G. 1983. Trophic structure of bird com- Rica: Barro Colorado Island, Panama; the mini- munities in forest patches in east-central Illinois. mum critical size of ecosystemsarea, Brazil; and Wilson Bull. 95416-430. Manu National Park. Peru. Yale Univ. Press.New BLAKE,J. G., AND J. R. KARR. 1984. Speciescom- Haven. position ofbird communities and the conservation LEVEY,D. J. 1986. Fruit-frugivore interactions in a benefit of largeversus small forests.Biol. Conserv. Costa Rican rain forest. Ph.D.diss. Univ. Wiscon- 30:173-187. sin, Madison. BLAKE,J. G., F. G. STILES,AND B. A. LOISELLE.In LEVEY,D. J. 1987. Facultative ripening in Hamelia mess. Birds of La Selva Biological Station: hab- Datens(Rubiaceae): effects of removal and rotting. itat use, trophic composition, and migrants. In A. becologia 74:203-208. Gentry [ed.], Four neotropical forests: a compar- LEVEY,D. J., ANDF. G. STILES.In press. Birds of La ison of La Selva. Costa Rica: Barro Colorado Is- Selva. In K. S. Bawa. G. S. Hartshorn. H. Hes- land, Panama; the minimum critical size of eco- penheide, and L. A. &Dade [eds.], La Selva- systemarea, Brazil; and Manu National Park, Peru. ecology and natural history of a lowland forest. Yale Univ. Press, New Haven. Sinauer Associates,New York. FETCHER,N., S. F. OBERBAUER,AND B. R. STRAIN. LOISELLE,B. A. 1987a. Migrant abundancein a Costa 1985. Vegetation effectson microclimate in low- Rican lowland forestcanopy. J. Trop. Ecol. 3: 163- land tropical forest in Costa Rica. Int. J. Biome- 168. teorol. 29: 145-155. LXXSELLE,B. A. 1987b. Birds and plants in a neo- FOGDEN,M.P.L. 1972. The seasonalityand popula- tropical rain forest: seasonalityand interactions. tion dynamics of equatorial forest birds in Sara- Ph.D.diss. Univ. Wisconsin, Madison. wak. Ibis 114:307-342. LOISELLE,B. A., AND J. G. BLAKE. In press. Diets of FOSTER,R. B. 1982. Famine on Barro Colorado Is- understory fruit-eating birds in Costa Rica: sea- land, p. 201-212. In E. Leigh, Jr., A. S. Rand, and sonality and resourceabundance. In M. L. Mor- D. Windsor leds.], The ecologyof a tropical forest. rison, C. J. Ralph, and J. Vemer [eds.], Food ex- Smithsonian Institution Press, Washington, DC. ploitation by terrestrialbirds. Stud. Avian Biology. FRANKIE. G. W.. H. G. BAKER.ANDP. A. OPLER. 1974. LOVEJOY,T. E. 1974. Bird diversity and abundance Comparative phenologicalstudies of trees in trop- in Amazonia forest communities. Living Bird 13: ical wet and dry forests in the lowlands of Costa 127-191. Rica. J. Ecology 62:881-919. LQWOY, T. E., R. 0. BIERREGAARD,JR., A. B. RYLANDS, GRADWOHL,J., AND R. GREENBERG.1980. The for- J. R. MALCOM,C. E. QUINTELA,L. H. HARPER,K. mation of antwren flocks on Barro Colorado Is- S. BROWN,JR., A. H. POWELL,G.V.N. POWELL, land, Panama. Auk 91~385-395. H.O.R. SCHUBART,AND M. B. HAYS. 1986. Edge GREENBERG,R. 1981. The abundanceand seasonality and other effects of isolation on Amazon forest of forest canopy birds on Barro Colorado Island, fragments,p. 257-285. In M. E. Soule [ed.], Con- Panama. Biotropica 13:24l-25 1. servation biology: the scienceof scarcity and di- HARTSHORN,G. 1983. Plants: introduction, p. 118- versity. Sinauer%ssociates,Sunderland,.MA. 157. In D. H. Janzen led.1. Costa Rican natural MARTIN. T. E.. AND J. R. KARR. 1986. Temnoral history. Univ. of Chicago Press, Chicago. dynamics of neotropical birds with special refer- HESPENHEIDE,H. 1971. Food preferenceand the ex- ence to frugivores in second-growthwoods. Wil- tent of overlap in some insectivorousbirds, with son Bull. 98:38-60. special reference to the Tyrannidae. Ibis 113:59- MUNN, C. A. 1985. Permanent canopy and under- 12. story flocksin Amazonia: speciescomposition and JANZEN,D. H. 1983. Insects: introduction, p. 619- population density, p. 683-7 12. In P. .A. Buckley, 645. In D. H. Janzen [ed.], Costa Rican natural M. S. Foster, E. S. Morton, R. S. Ridgely, and F. history. Univ. of Chicago Press, Chicago. G. Buckley [eds.], Neotropical ornithology. Or- 170 BETTE A. LOISELLE
nithol. Monoar. No. 36, American Ornithologists’ STILES,F. G. 1978. Temporal organization of flow- Union, Washmgton, DC. ering among the hummingbird food plants of trop- MUNN. C. A.. AND J. W. TERBORGH.1979. Multi- ical wet forest. Biotropica 10:194-2 10. speciesterritoriality in neotropical foragingflocks. STILES,F. G. 1980. The annual cycle in a tropical wet Condor 81:338-347. forest hummingbird community. Ibis 122:322- OPLER,P. A., G. W. FRANKIE,AND H. G. BAKER. 1980. 343. Comparative phenological studies of treelet and STILES,F. G. 1983. Birds: Introduction, p. 502-530. shrub speciesin tropical wet and dry forestsin the In D. H. Janzen [ed.], Costa Rican natural history. lowlands of Costa Rica. J. Ecol. 68: 167-l 88. Univ. Chicago Press, Chicago. PEARSON,D. L. 1971. Vertical stratification of birds STILES,F. G. 1985. Seasonalpatterns and coevolution in a tropical dry forest. Condor 73:46-55. in the hummingbird-flower community of a Costa PEARSON,D. L. 1975. The relation of foliage com- Rican subtouicalforest, D. 757-785. In P. A. Buck- plexity to ecologicaldiversity of three Amazonian ley, M. S. Foster, E. S. Morton, R. S. Ridgely, and bird communities. Condor 77~453466. N. G. Smith [eds.], Neotropical ornithology. Or- PEARSON,D. L. 1977. Ecologicalrelationships of small nithol. Monogr. No. 36. American Ornithologists’ antbirds in Amazonian bird communities. Auk Union, Washington, DC. 94~283-292. WHEELWRIGHT,N. T. 1983. Fruits and the ecology PERRY,D. R. 1978. A method of accessinto the of Resplendent Quetzals. Auk 100:286-301. crowns of emergent and canopy trees. Biotropica WHEELWRIGHT,N. 1986. A seven-year study of in- 10:155-157. dividual variation in fruit production in tropical PERRY,D. R., AND A. STARRETT.1980. The polli- bird-dispersed tree species in the family Laura- nation ecology and blooming strategy of a neo- ceae, p. 21-36. In A. Estrada and T. H. Fleming tropical emergenttree, Dipteryxpanamensis.Bio- [eds.], Frugivores and seed dispersal. Junk Pub- tropica 12:307-3 13. lishers, Dordrecht, The Netherlands. RIDOELY,R. S. 1976. A guide to the birds of Panama. WIENS,J. A. 1977. On competition and variable en- Princeton Univ. Press, Princeton. vironments. Am. Sci. 65:590-597. SHAPIRO,S. S., AND M. B. WILK. 1965. An analysis WILLIS,E. 0. 1979. The composition of avian com- of variance test for normality (complete samples). munities in remanescent woodlots in southern Biometrika 52:591-611. Brazil. Papeis Avulsos de Zoologia 33: l-25. SHERRY,T. W. 1983. Monasa morphoeus:species WILLIS, E. O., AND E. EISENMANN. 1979. A revised accounts,p. 587-590. In D. H. Janzen [ed.], Costa list of birds of Barro Colorado Island, Panama. Rican natural history. Univ. Chicago Press, Chi- Smithson. Contrib. Zool. 29 1:l-3 1. cago. WOLDA,H. 1978. Fluctuationsin abundanceof trop- SKUTCH,A. 1972. Studiesof tropical American birds. ical insects.Am. Nat. 112:1017-1045. Publ. Nuttall Omithol. Club lO:l-228. WOLDA,H. 1982. SeasonalityofHomopteraon Barro SMYTHE.N. M. 1982. The seasonal abundance of Colorado Island. D. 319-330. In E. L&h. Jr.. A. night-flying insectsin a neotropical forest, p. 309- S. Rand, and D.‘Windsor [eds.], The ecology of a 3 18. In E. Leigh, Jr., A. S. Rand, and D. Windsor tropical forest. Smithsonian Institution Press, [eds.], The ecology of a tropical forest. Smithson- Washington, DC. ian Institution Press, Washington, DC. WONG,M. 1986. Trophic organization of understory SOKAL,R. R., AND F. J. ROHLF. 1981. Biometry. W. birds in a Malaysian dipterocarp forest. Auk 103: H. Freeman and Co., San Francisco. 100-l 16. SEASONALITY IN CANOPY BIRDS 771
APPENDIX. Number of individuals recorded over APPENDIX. Continued. all dates from censusesconducted in Dipteryx (Tree 1) and Hymenolobium(Tree 2) during 1985-l 986. Guilds Number of are describedin the text. English and scientific names individuals follow American Ornithologists’ Union (1983, 1985). Swcies Tree 1 Tree 2 Collared Aracari Number of individuals Pteroglossustorquatus 69 42 Species Tree I Tree 2 Yellow-eared Toucanet - Selenideraspectabilis 0 8 Scavengers Keel-billed Toucan King Vulture Ramphastossulfuratus 82 44 Sarcoramphuspapa 2 0 Chestnut-mandibled Toucan R. swainsonii 17 43 Raptors Purple-throated Fruitcrow Double-toothed Kite Querula purpurata 42 15 Harpagus bidentatus 8 0 Bare-neckedUmbrellabird Tiny Hawk Cephalopterusglabricollis 5 1 Accipitersuperciliosus 0 1 Three-wattled Bellbird SemiplumbeousHawk Procniastricarunculata 4 6 Leucopternissemiplumbea 9 9 Chestnut-headedOropendola Laughing Falcon Psarocoliuswagleri 74 65 Herpetotherescachinnans 6 4 Montezuma Oropendola Slaty-backedForest-Falcon P. montezuma 101 58 Micrastur mirandollei 0 2 Collared Forest-Falcon Small frugivores A4. semitorquatus 1 0 Olive-striped Flycatcher Mionectesolivaceus 2 0 Seed eaters (parrots) Boat-billed Flycatcher Crimson-fronted Parakeet Megarynchuspitangua 7 1 Aratinga jinschi 2 0 Gray-capped Flycatcher Olive-throated Parakeet Myiozetetesgranadensis 18 0 A. nana 2 0 Masked Tityra Aratinga sp.” 1 0 Tityra semtjasciata 48 13 Orange-chinnedParakeet Black-crowned Tityra Brotogerisjugularis 23 5 T. inquisitor 6 2 Brown-hooded Parrot Rufous Piha Pionopsittahaematotis 26 47 Lipaugus unirufus 44 19 White-crowned Parrot Snowy Cotinga Pionus senilis 106 31 Carpodectesnitidus 26 15 Red-lored Parrot Red-capped Manakin Amazona autumnalis 44 29 Pipra mentalis 0 1 Mealy Parrot Yellow-throated Vireo A. farinosa 131 90 Vireojlavifrons 1 0 Nectarivores Red-eyed Vireo V. olivaceus 6 6 Long-tailed Hermit Bay-breastedWarbler Phaethornissuperciliosus 2 1 Dendroicacastanea 2 5 White-necked Jacobin Plain-colored Tanager Florisuga mellivora 4 3 Tangara inornata 2 0 Crowned Woodnymph Golden-masked Tanager Thalurania colombica 35 24 T. larvata 4 3 Purple-crowned Fairy Yellow-crowned Euphonia Heliothryx barroti 0 8 Euphonia luteicapilla 14 3 Hummingbird species 4 11 Olive-backed Euphonia Large frugivores E. gouldi 80 44 Crested Guan White-vented Euphonia Penelopepurpurascens 5 7 E. minuta 13 3 Short-billed Pigeon White-shouldered Tanager Columba nigrirostris 74 48 Tachyphonusluctuosus 14 19 Slaty-tailed Trogon Tawny-crested Tanager Trogon massena 38 23 T. delatrii 12 1 Lattice-tailed Trogon Summer Tanager T. clathratus 1 1 Piranga rubra 1 2 712 BETTE A. LOISELLE
APPENDIX. Continued. APPENDIX. Continued.
Number of Number of individuals individuals Tree 1 Tree 2 Snecie~ Tree I Tree 2 Species
Slate-coloredGrosbeak Black-cappedPygmy-Tyrant Pitylus grossus 32 23 Myiornis atricapillus 16 5 Black-facedGrosbeak Yellow-margined Flycatcher Caryothraustespoliogaster 4 2 Tolmomyias assimilis 21 14 Scarlet-rumped Cacique Contopussp. 2 2 Cacicusuropygialis 93 59 Empidonax sp. 1 4 Rufous Mourner Large insectivores Rhytipterna holerythra 13 13 Squirrel Cuckoo Great Crested Flycatcher Piaya cayana 27 14 Myiarchus crinitus 2 0 White-necked Puflbird White-ringed Flycatcher Bucco macrorhynchus 6 2 Coryphotriccusalbovittatus 42 1 White-fronted Nunbird Cinnamon Becard Monasa morphoeus 39 23 Pachyramphuscinnamomeus 1 0 Chestnut-coloredWoodpecker Tropical Gnatcatcher Celeuscastaneus 13 10 Polioptila plumbea 52 26 Lineated Woodpecker Lesser Greenlet Dryocopuslineatus 1 1 Hylophilus decurtatus 12 11 Pale-billed Woodpecker Green Shrike-Vireo Campephilusquatemalensis 32 14 Vireolaniuspulchellus 8 0 Small insectivores Chestnut-sidedWarbler Dendroicapensylvanica 24 12 Black-cheekedWoodpecker Blackbumian Warbler 3 2 Melanerpespucherani D. fusca 2 1 Smoky-brown Woodpecker 0 1 2 0 Dendroica sp. Veniliornisfumigatus Canada Warbler Rufous-wingedWoodpecker Wilsonia canadensis 1 0 Piculus leucolaemus 0 1 Cinnamon Woodpecker Frugivore-nectarivore-insectivores Celeusloricatus 9 2 TennesseeWarbler Woodpecker sp.= 1 4 Vermivoraperegrina 11 4 Striped Woodhaunter Blue Dacnis Hyloctistessubulatus 1 0 Dacnis cayana 12 11 Wedge-billed Woodcreeper Green Honeycreeper Glyphorhynchusspirurus 1 0 Chlorophanesspiza 14 7 Barred Woodcreeper Shining Honeycreeper Dendrocolaptescerthia 1 0 Cyanerpeslucidus 38 18 Black-striped Woodcreeper Northern Oriole Xiphorhynchuslachrymosus 39 23 Icterus galbula 2 4 Paltry Tyrannulet Zimmerius vilissimus 1 4 8 Not counted as a separate species.