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This content downloaded from 128.171.57.189 on Mon, 13 May 2013 21:28:23 PM All use subject to JSTOR Terms and Conditions The Condor91:891-907 ? The CooperOrnithological Society 1989

BIRDUSE OF EPIPHYTERESOURCES IN NEOTROPICALTREES

NALINIM. NADKARNI2AND TERIJ. MATELSON Departmentof BiologicalSciences, University of California,Santa Barbara, CA 93106

Abstract. Epiphytesare a commoncomponent of neotropicalforests, but theirimpor- tanceto birdsat thecommunity level and their role in contributingto tropicalbird diversity hasonly rarely been considered. Literature accounts from 55 studiesdocument 193 species of neotropicalbirds that take nectar, fruits, invertebrates, water, and nesting materials from .To quantifythe amounts and types of resourcesprovided by epiphytescompared to hosttrees, we watchedbirds in 14 forestand pasture sites (1,350-1,420 m) for2 months in a lowermontane landscape of CostaRica. During our 289 hrof observationsfrom within the canopyand on the ground,33 of 56 birdspecies observed in foragingvisits foraged in resourcesprovided by epiphytes. resources were involved in 32%of all foraging visits.For eight species, 40% or moreof allforaging visits involved epiphyte use, which includedforaging for fruits, nectar, invertebrates, water, and nesting materials. Six typesof birdforaging behaviors in six typesof epiphytesare described and compared to birduse of treeresources. Some appeared to specializeon particularepiphyte resources such as invertebratesin crownhumus. The frequent epiphyte use by a largenumber of birdspecies indicatesthat epiphytes constitute a resourcethat has generally been overlooked in pastbird communitystudies. We discusstwo waysthat epiphytes may contribute to hightropical birdspecies diversity. Key words: Epiphytes;canopy; ; tropical forest; foraging ecology; resource; Monteverde;Costa Rica; community ecology.

INTRODUCTION which supportscanopy humus invertebrates,in- Studies of relationshipsbetween tropical forest cluding earthworms, millipedes, beetles, and birdsand plantshave focusedalmost exclusively other (Lyford 1969, Nadkarni and on resourcesprovided by and understory Longino 1988). shrubs.Epiphytes, that derive supportbut Given the greatdiversity and largebiomass of not nutrients from their host trees, are a con- epiphytes in tropical and temperatewet forests spicuous component of many tropical and wet (Nadkarni1984, 1985;Gentry and Dodson 1987), temperateforests. They occupy the same phys- thereis surprisinglylittle data on their use by the ical location as their host trees and produce a animalcommunity. Only a few field studieshave diverse arrayof fruits, nectar, and foliage (Ben- mentioned(Orians 1969) or quantified(Remsen zing 1987, Gentry and Dodson 1987). Epiphyte 1985) the importance of epiphytes, (primarily biomass varies greatlyamong forest types; it is ) as a resourcefor tropicalbirds. Only one largestin neotropicalcloud forests,where the live study has directlycompared temperate vs. trop- and dead standingcrop can exceed 4,800 kg/ha, ical epiphyte use by birds (Thiollay 1988). A equivalent to 40% of the total , shrub, and numberof studiesfocusing on the use of canopy- understoryfoliar biomass (Nadkarni 1984). Many held dead-leaflitter pointed out the need to dis- tank and rosette epiphytes impound and store tinguish within-canopyresources (Remsen and water, leaf litter, and dissolved and particulate Parker 1984). However, nearly all the informa- minerals, which support populations of inver- tion is scatteredin general descriptionsof bird tebrates and vertebrates(Picado 1911, Laessle behavior and resource use. The technical diffi- 1961).The dead organicmatter that accumulates culties of observingbirds within the canopyitself beneath mats of live epiphytic cryptogams have been overcome in only very few studies by (mosses and liverworts)creates a microhabitat using towers,walkways, and mountain-climbing equipment (e.g., Perry 1978, Greenberg 1981, Loiselle 1987). Although a large body of litera- 'Received15 February1989. Final acceptance 26 ture on July1989. epiphyte , physiology, and 2 Presentaddress: Director of Research,The Marie mineral nutrition exists (Watson et al. 1987), SelbyBotanical Gardens, 811 SouthPalm Avenue, ecological interactions of birds and canopy- Sarasota,FL 34236. dwelling plants have been almost entirely over- [891]

This content downloaded from 128.171.57.189 on Mon, 13 May 2013 21:28:23 PM All use subject to JSTOR Terms and Conditions 892 NALINIM. NADKARNIAND TERI J. MATELSON looked in the literature,except for a few groups (ovenbirds, 14 species),Tyrannidae (flycatchers, such as the hummingbirds(e.g., Feinsingeret al. 14 species), Fringillidae(finches, 8 species), Pa- 1987) and several frugivorousspecies that dis- rulidae (warblers, 8 species), and Turdidae persemistletoes (e.g., Davidar 1983, Fitzpatrick (thrushes,7 species).Nesting materialsfrom epi- 1980, Parker1981, Remsen et al. 1982). phytes have been noted anecdotally for many This studyis a firststep in assessingthe overall species of birds, and are most commonly col- importanceof epiphytes to birds in the tropics. lected by Furnariidae. We summarize scatteredliterature accounts of Epiphyteresources used by birdsinclude fruits, epiphyteuse by birdswith respectto bird species, flowers, seeds, water, and invertebratesin bro- resource types, and epiphyte groups involved. meliad "ponds"and sequesteredin dead organic We then present results of a field study that fo- matterbeneath mats, nestingmaterials, and cused on bird and epiphyte interactionsin trees nest sites. The most frequentcitations concerned of primaryforests and pasturesin Monteverde, foragingfor epiphyticfruits and nectarin flowers Costa Rica, to ask the following questions: (1) (Table 1 and Appendix 1). The list of epiphytes What species of birds are associated with epi- used by birds includes 42 genera in 15 families phyteuse? (2) Whatis the frequencyof bird visits of vascularand nonvascularplants (Table 1).The and foragingbehavior associatedwith resources , Loranthaceae, Marcgraviaceae, createdby epiphytes comparedto those of host and Ericaceaeare the families of vascular epi- trees? (3) Which epiphyte groups and epiphyte phytes most frequentlycited for use by birds. resourcesare used by the bird community?(4) Do any birds appearto specialize on particular FIELD STUDY OF EPIPHYTE resourcesprovided by epiphytesor on particular USE BY BIRDS epiphytegroups? (5) What are community-level STUDYAREA implicationsof bird exploitationof epiphyte re- sources? Study sites were in Monteverde, Puntarenas Province, Costa Rica (10018'N, 84048'W).The LITERATUREREVIEW OF EPIPHYTE area is a mosaic of primarylower montane wet USE BY BIRDS forest and pasturesof various land-use histories We searchedthe literaturefor any referencescon- (Lawtonand Dryer 1980). The bird community cerningneotropical bird use of epiphytes(except of Monteverdehas been well studied, and bird- for field identificationguides, which almost ex- plantinteractions have receivedparticular atten- clusively describeforaging behaviors anecdotal- tion (e.g., Wheelwrightet al. 1984, Feinsingeret ly). We reviewed 55 papers that fell into four al. 1987). We selected 14 sites between 1,350 categories:(1) frugivoryin neotropicalbirds, (2) and 1,420 m in elevation and within 2 km of hummingbirdpollination, (3) bird life-histories, each other. These sites represent the range of and (4) mistletoe dispersal (Appendix 1). This in the area: (a) three sites in primary compilationis usefulin identifyinggeneral trends lower montane forest,(b) five sites in "relicttree and documentingthe diversity of birds that use pastures"(pastures partially cut, leaving some epiphytes.The extentto which this summarycan primaryforest trees), and (c) six sites in "scrub be generalizedto a community level is limited, tree pastures"(pastures cut completely, with a however,as it reflectsthe purposesand geograph- similardensity of second-growthtree speciescol- ical locations of studies not specificallydesigned onizing the pastures).Differences in bird use of to assess the importanceof epiphytes to birds. epiphytesin the three habitatswill be described A total of 193 species of birds in 125 genera elsewhere(Nadkamrni and Matelson, unpubl.) and 25 familieshas been cited as using epiphytes Epiphytesof the Monteverdecommunity are (Appendix 1). Birds of the three major diet cat- describedin Nadkamrni(1986). The taxonomyand egories (frugivores, insectivores, and nectari- distributionofepiphytes are in generalonly poorly vores) are representedin approximatelyequal known, and no quantitativeassessment of epi- proportions.Bird families most frequentlycited phyte abundancein particularhabitats or on in- as users of epiphytes are the Thraupidae(tana- dividualtrees in Monteverdeare currentlyavail- gers) and Trochilidae (hummingbirds),52 and able. We categorizedthe diverse community of 37 species, respectively.Other major bird fam- epiphytes into six groups: (1) woody shrubs- ilies that use epiphyte resourcesare Furnariidae mainly species of Cavendishia,Gonocalyx, Dys-

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TABLE1. Birduse of epiphytesby plantgroup and resourcetype, based on informationfrom 55 published reports.A totalof 193bird species have been recorded to use epiphytes.Epiphyte resource type: In = inver- 11 F tebrates;Fl = flowers (mainly nectar);Fr = fruits or seeds;Ne = nestingmaterial, nest sites, or nestcover; D Wa = water. G

Number of bird species using epiphytes Plantgroup Resourcetype 58 Bromeliacae In Fl Fr WaNe 53 Bryophyta In N Wa C 50 Loranthaceae Fl Fr 39 Marcgraviaceae In Fl Fr 18 Ericaceae Fl Fr Ne 12 Gesneriaceae Fl Fr G 9 Guttiferae Fl Fr A7 8 Solanaceae Fr 6 Araceae Fr Ne 6 Araliaceae Fr 5 In Ne 5 Fr Ne 5 Cactaceae Fr 3 Pteridophyta Ne 1 Begoniaceae Ne 1 Piperaceae Ne A 1 Rubiaceae Fr

FIGURE 1. Epiphyte mat. A = branch, B = dead terigma, and Satyria (Ericaceae), Lycianthes organicmatter, C = bromeliads,D = ericaceousshrub synthera (Solanaceae),Hillea spp. (Rubiaceae), (woodyshrub), E = mosses and filmy ,F = orchid G = Noranteacostaricensis (Marcgraviaceae), Clusia (herbaceousplants), ferns. spp. (Guttiferae),and Didymopanaxsp. (Arali- aceae):(2) tank bromeliads-species of Tilland- observers familiar with resident birds and the sia, Guzmania, and Vriesia(Bromeliaceae); (3) vegetation of the area. At each of the 14 sites, herbaceousepiphytes-species of the Orchida- we establisheda semicircularobservation arena, ceae, Begoniaceae,Gesneriaceae, Araceae, Cac- approximately30 m in radius, that contained taceae, Peperomia (Piperaceae),and ferns; (4) nine to 17 trees (X = 12, SD = 5.1). Separate mistletoes (Loranthaceae)(although they are not observersrecorded bird activities in forest and true epiphytes,they are includedas they provide pasture sites simultaneously. Observation ses- canopy resources distinct from host trees); (5) sions, distributed evenly throughoutthe study dead organicmatter, lichens, mosses, and other period,were 3 hr long, with two sessions per day, cryptogamswhich make up interwoven moss- between 06:00 and 18:00, as weatherpermitted. -humusmats of"crown humus" (Jenik 1973); The total amount of observation time in forest and (6) other epiphytes-unknown vascularand and pasture(relict plus scrub pasture)sites was nonvascularplants (Fig. 1). In general,forest and nearlyequal (140 and 149 hr, respectively),and relict pasture tree-crowns supported large all direct comparisons have been correctedfor amountsofcryptogams and dead organicmatter, the discrepancy(3%) in observationtime. woody shrubs,and herbs;epiphyte communities In forestsites two observerswere needed. One in scrubpastures were dominated by xerophytic watchedunderstory birds by walkingaround the shrubs and herbs, mistletoes, and tank brome- peripheryof the arena on the ground. Another liads (pers. observ.). observer, suspended on a portable platform 25 METHODSOF OBSERVATIONS m above the forest floor (Nadkarni 1988), re- cordedbirds in the canopy.Tree-climbing meth- Observationsof bird activities were carriedout ods followedthose of Perry(1978). Ourpresence daily from I July to 28 August 1985 by three in the canopy did not appear to affect bird be-

This content downloaded from 128.171.57.189 on Mon, 13 May 2013 21:28:23 PM All use subject to JSTOR Terms and Conditions 894 NALINIM. NADKARNIAND TERI J. MATELSON havior, because birds perched, vocalized, and The proportionof epiphytevisits relativeto host foragedon brancheswithin 1 m of the platform. tree visits variedwith bird species(Table 2). Bird In pasturesites, a single observeron the ground species that used epiphyte resources most fre- had an unobstructedview of the entire arena. quently were hummingbirds,tanagers, and fly- We recordedthe numberof birds that alighted catchers.Birds which were seen in our sites and on trees in our sites, and noted whether they which did not use epiphytesare listed in Appen- perched,vocalized, or foraged.In this paper,we dix 2. discuss only those visits that involved foraging The foraging behaviors associated with epi- activitiesof birdsin treesor epiphytes.The "vis- phytic resources differed from behaviors asso- it," our unit of epiphyte or host tree use, was ciated with host tree resources (Fig. 2). Thirty defined as an individual bird exhibiting any of percent of the epiphyte visits involved special- the foragingbehaviors (following Remsen and ized epiphyteforaging behaviors (probing in moss Robinson, unpubl.) listed below for more than mats and probing bromeliads for water or in- 2 sec. For each visit, we noted bird species, vertebrates)that have no host tree counterpart. whetherit used a host tree or an epiphyte (and, For the four other foragingcategories, the pro- for the latter,epiphyte group used), and foraging portionsdiffered significantly, using contingency behaviors:(1) collecting or consuming fruit, (2) table analysis (x2 = 70.7, df = 3, P < 0.001); probing flowers or hovering at extrafloralnec- proportionately,birds foraged more frequently taries for nectar, water, or invertebrates, (3) on epiphyteflowers than on host tree flowers.A gleaning foliage for invertebrates,(4) probing greaterproportion of foragingvisits was spent in moss mats and crown humus for invertebrates general searching(no immediate food acquisi- or water, (5) probingbromeliad tanks for inver- tion) in host trees than in epiphytes. tebratesor water, and (6) general searchingbe- The most commonly used epiphyte type was havior that resultedin no immediate use or re- woody shrubs, and the least common was her- moval of material. The latter category was baceousepiphytes (Fig. 3). Of the birds that used somewhat subjective,but we distinguishedgen- epiphytes frequently(Table 2), some appeared eral searchingbehavior from other uses if there to forage preferentiallyin particular epiphyte was no bill contact with the substrate.General types. We used contingencytable analysisto test searchingwas distinguishedfrom mere perching whetherthe relativeproportions of epiphytetypes if birds exhibited behaviors that we recognized used by each of these species differedfrom the as precedinga collecting or feeding event such proportionsused by all species combined. (We as hovering, hopping near, or closely observing subtractedthe visits of the species in question fruit, flowers,extrafloral nectaries, or barkcrev- from the total). Five species differedsignificantly ices. Bird nomenclaturegenerally follows Meyer (P < 0.01) from the bird community as a whole de Schauensee(1970) and the AOU check-list in the relative proportions of epiphyte groups (1983). used (Fig. 3). The White-throatedMountain-gem used flowers of ericaceous shrubs significantly more frequentlythan expected;the Ochraceous RESULTS Wren and Common Bush-Tanagerforaged in Seventy-onespecies of birdsvisited our sites dur- dead organicmatter and mosses more frequently, ing the study period. Of the 56 bird species that and the Golden-browedChlorophonia and Ol- foragedin our sites, 33 species (59%)used epi- ive-striped Flycatcher fed on mistletoes more phytic resources.We are confidentthat our ob- frequentlythan expected. servationsencompassed the true composition of Because our field season spanned only 2 the bird communityduring the study period,be- months, we cannot ascertain if any birds spe- cause we observed 37 of the total 56 species by cialized on epiphytes over host tree resources the end of the first30 days of the study, and only duringthe entire year. However, two species of four additional species were recorded between birds exhibited almost exclusive use of a single day 40 and the end of the 60-day study. epiphyte type during the study: the Variable We recordeda total of 3,473 visits (perching, Mountain-gem used woody shrubs, and the vocalizing, and foraging),of which 1,935 (56%) OchraceousWren foraged in dead organicmatter involved foragingbehavior. Overall, 620 (32%) for over 90%of their epiphytevisits. These two of these foraging visits involved epiphyte use. bird species had the highest proportionof epi-

This content downloaded from 128.171.57.189 on Mon, 13 May 2013 21:28:23 PM All use subject to JSTOR Terms and Conditions BIRDUSE OF EPIPHYTES 895 phyte visits of all bird species (97%and 89% of as probinginto moss mats and bromeliadtanks all foragingvisits, respectively,Table 2). is unknown,the size of this underestimationcan- Seven species of birds appearedto specialize not be quantifiedwith these data. on particulartypes of epiphytes;i.e., even if they This potential underestimation of total re- did not use epiphytes as the major part of their sources availableand used by birds has only in- total resource use, over 90% of their epiphyte frequentlybeen consideredin discussions of the visits involved particularepiphyte types (Table latitudinalgradient of bird diversity.The greater 3A). Five other specieswere consideredepiphyte diversityof birdsin tropicalvs. temperateforests generalists,using at least four of the five epiphyte has been attributedto various aspects of types,with no morethan 40% in any one category diversity and resource availability (MacArthur (Table 3B). and MacArthur1961; Orians 1969; Karr 1971, Specializationat a fine spatial scale occurred 1975;Karr and Roth 1971;Lovejoy 1971;Rech- for one genus of epiphyte, which was used in a er 1971;Terborgh 1971; Stiles 1985). The higher variety of ways by six bird species. In one of our diversity in tropical forests has most often been forest sites, a woody epiphytic shrub, Norantea linked to the greatercomplexity of tropicalforest sp., (Marcgraviaceae)covered approximately5 structure,particularly with structuralindices such m ofa horizontalDussia sp. (Leguminoseae)tree as foliage height diversity (MacArthur and branch (diameter= 25-30 cm) 23 m above the MacArthur 1961; Terborgh and Weske 1969; forest floor. We estimated that the shrub held Karr 1971; Pearson 1971, 1977; Recher 1971; between300 and 350 fruitsthat ripenedthrough- Willson 1974). Another factor to explain higher out our study period, turningfrom light greento tropical bird diversity is the presenceof certain red in color. We observed six species of birds resource elements in tropical forests that have usingthe shrub:Slate-throated Redstarts gleaned no counterpartin temperateforests. Examples of its foliage;Silver-throated Tanagers and Emerald "new resources"(Karr 1975) that are exploitable Toucanetsfed upon its fruits;Stripe-tailed Hum- in tropical but not temperate forests and that mingbirdsand VariableMountain-gems visited enhance particularbird species or guilds of bird extrafloralnectaries; and Prong-billed Barbets species include large insects (Schoener 1971), gleaned branches. army ants (Willis and Oniki 1978), bamboo thickets(Parker 1982), oxbow lake edge and per- DISCUSSION manently flooded forest (Remsen and Parker Ourliterature search and fieldobservations sum- 1983), and suspendeddead leaves (Remsen and marize what is currentlyknown about the use of Parker 1984). epiphytes by tropical birds. Patterns described An abundantepiphyte community contributes for the largergeographical areas encompassed in both to the vertical structuraldiversity of forest the literaturewere consistent with results from vegetationand to the amountsand types of food the montanelandscape of Monteverde.A diverse and energy resourcesavailable to . We assemblage of birds use epiphyte-derived re- suggest two mechanisms by which epiphytes sourceswhen foraging for nutrients,energy, water, might maintainor enhancebird speciesdiversity and nesting materials. at the community level: (1) epiphytes swell the If the proportionof foragingvisits to a resource canopy resource pool by producing additional is a generalindicator of its importanceto birds, resourcesthat are "auxiliary"to those created our results suggest that the total resource pool by host trees, and which may enhance oppor- available to birds in tropical forests is underes- tunities for resourcespecialization, and (2) phe- timated if epiphyte resourcesare discounted or nologicaldifferences between epiphytes and their only qualitativelydescribed. One-third of all vis- hosts make some epiphyteresources available to its that we classified as foraging involved re- birds at a differenttime of the year than those sources created by epiphytes. The actual re- provided by host trees. sources obtained from epiphytes may be even greater compared to those obtained from host MECHANISM1: PRODUCTION OF AUXILIARY trees, because a larger proportion of tree visits RESOURCES were "general searching,"a behavior that re- In moist and wet tropicalforests, epiphyte species sulted in no immediate reward.However, since constitute 34%to 63%of all species (Gen- the chanceof prey acquisitionby such behaviors try and Dodson 1987). Their diverse growth-

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TABLE2. Percentageof foragingvisits to epiphytesby birdsin the Monteverdefield study, 1 July to 28 August 1985. Frequentforagers had 10 or more foragingvisits recordedduring the study period. Infrequentforagers had less than 10 foragingvisits recorded.Foraging behavior (in descendingorder of frequencyof use): B = probingbromeliads, Dm = probingmoss mats and dead organicmatter, Fg = gleaningfoliar and stem surfaces, Fl = probingor hovering at flowersor extrafloralnectaries, Fr = gatheringor consumingfruit, Gs = general searchingwith no immediate resourceuse.

%(Total number) foraging visits Birdspecies to epiphytes Foragingbehavior Frequentforaging visits (>10 foragingvisits) White-throatedMountain-gem Lamporniscastaneoventris 95 (150) FI Gs Dm Fr Fg OchraceousWren Troglodytesochraceus 89 (19) Dm B FI Stripe-tailedHummingbird Eupherusaeximia 71 (14) FI Fg Common Bush-Tanager Chlorospingusophthalmicus 57 (511) Dm FI Fg Fr Gs B Olive-stripedFlycatcher Mionectesolivaceus 46 (37) Fr Fl Gs Fg Dm Slate-throatedRedstart Myioborusminiatus 45 (47) Fg Dm Gs Fl Yellow-throatedBrush-Finch Atlapetesgutturalis 31 (13) Fg Prong-billedBarbet Semnornisfrantzii 30 (23) Fr Fl Gs Dm Golden-browedChlorophonia Chlorophoniacallophrys 33 (187) Fr Dm Gs B House Wren Troglodytesaedon 26 (57) Dm B Gs Fg Fr Three-stripedWarbler Basileuterustristriatus 20 (10) Dm PaltryTyrannulet Zimmeriusvilissimus 15 (61) Gs Fg Scarlet-thighedDacnis Dacnis venusta 14(256) B Fr Fl Silver-throatedTanager Tangaraicterocephala 13 (78) Fl Fr Yellow-throatedEuphonia Euphoniahirundinacea 13 (16) Fg Fork-tailedEmerald Chlorostilboncanivetii 10 (20) Fl Brown-cappedVireo Vireoleucophrys <10(13) Gs EmeraldToucanet Aulacorhynchusprasinus <10 (93) Fr MountainElaenia Elaeniafrantzii <10 (30) Gs MountainRobin Turdusplebejus <10 (146) B Dm Dusky-cappedFlycatcher Myiarchustuberculifer <10 (50) B Infrequentforagers (<10 total foragingvisits) Boat-billedFlycatcher Megarynchuspitangua Fg Orange-belliedTrogon Trogonaurantiiventris B BrownJay Cyanocoraxmorio B Spotted Barbtail Premnoplexbrunnescens Dm Coppery-headedEmerald Elvira cupreiceps Fl

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TABLE2. Continued.

%(Total number) foraging visits Birdspecies to epiphytes Foragingbehavior Green-crownedBrilliant Heliodoxajacula Dm Hepatic Tanager Pirangaflava Dm Black-facedSolitaire Myadestesmelanops Gs Sooty-cappedBush-Tanager Chlorospinguspileatus B Tufted Flycatcher Mitrephanesphaeocercus Gs Violet Sabrewing Campylopterushemileucurus Fl White-earedGround-Sparrow Melozone leucotis Dm All species 32 (1,935) forms increase the spatial complexity of tree study, four of the 56 species foragingin our sites crowns. Their live and dead components create (7%)used epiphytesfor more than 50%of their microhabitatsthat support communities of in- foraging(Table 2). This is similar to Remsen's vertebratesand vertebratesthat do not exist in (1985) data from Bolivia, where four of the 80 trees and forestsdevoid of epiphytes.Bromeliad montane bird species (5%)are epiphyte special- tanks that impound waterand litter and support ists. These ideas concur with those of Remsen animals are used by at least 58 species of birds and Parker(1984), who documentedguilds of as (Table 1, Appendix 1). Forty-fourbird species many as eight sympatricbird species that forage forage for invertebratesin crown humus con- tained in neotropicalforest trees (Appendix 1). Structurallyand taxonomically diverse habi- tats also provide greater opportunities for re- I 1O0 2 141 243 6___3 18._ 17. _ source subdivisionand thereforegreater bird di- versity in many habitats (Orians 1969, S80 MacArthur1970, Cody 1974, Karr 1975). In our 60

LL 40

20 S100 ALL VMG CBT CHL OWR OSF

BIRDSPECIES S60 b 820 FIGURE3. Birduse of the six epiphytetypes in Mon- " 40- ,.c O40.... I IIII II i teverde duringthe study period. The six bird species TREEEPIPHYTEz presentedare the most common species that used epi- 20 phytesfor at least 30%of theirtotal foragingvisits and that differedsignificantly from the overall bird com- TREE EPIPHYTE munity in the proportionof types of epiphytes used. VMG = White-throatedMountain-gem (Lampornis FIGURE 2. Foragingbehavior of birds associated castaneoventris); CBT = Common Bush-Tanager with tree and epiphyteresources during the study pe- (Chlorospingusophthalmicus); CHL = Golden-browed riod. fr = collectingand/or consumingfruit; fl = prob- Chlorophonia (Chlorophonia callophrys); OWR = ing or hoveringat flowersor extrafloralnectaries; fo = OchraceousWren (Troglodytes ochraceus); OSF = Ol- gleaningfoliage; b = probingbromeliad tanks and leaf ive-stripedFlycatcher (Mionectes olivaceus). Epiphyte bases; m = probingmoss mats and crown humus;gs types are describedin the text: w = woody shrubs;d = generalsearch with no immediateuse or removal of = dead organicmatter and mosses; b = bromeliads;p material.Total number of foragingvisits is shownabove = parasitesand mistletoes;h = herbaceousepiphytes; each bar. m = miscellaneousand unidentifiedepiphytes.

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TABLE3. Birdspecies exhibiting (A) specialized and 44 trees in our three forest interiorsites were in (B)generalized use of the five typesof epiphytesde- fruit or flower. However, many of the woody scribedin thetext. Only those species with more than five visits are presented.(A) Specialistsused the in- epiphytic shrubs (including the Norantea de- dicatedepiphyte type for 90% or more of theirepiphyte scribed above) were in flower or fruit and were visits.(B) Epiphytegeneralists used at leastfour epi- used for 40% of all foragingvisits (Fig. 3). phytetypes in similarproportions (no one epiphyte The volume and biomass of epiphytes, then, typeexceeded 40% of totaluse). may be farsmaller than host trees,but the timing of their resourcesmay differin crucialways. We Epiphytetype Birdspecies proposetwo temporaleffects that could maintain A. Specialists or enhancebird species diversity in forests with Woodyshrubs White-throated well-developed epiphyte communities. First, Mountain-gem resources functionas EmeraldToucanet epiphytic may supplements Silver-throated during "lean times" of trees and understory Tanager plants,producing flowers, fruits, and leaves con- Three-striped tinuously (or asynchronously)throughout the Warbler year. Second, certain epiphytes such as mosses, Mossmats and OchraceousWren bromeliad tanks, and canopy humus may pro- crownhumus SpottedBarbtail' vide microhabitatsfor invertebrates,which ap- Bromeliads BrownJay' pear to be less seasonal than habitats provided B. Generalists by the canopy tree alone. Golden-browed Epiphyticcommunities occur in a wide range Chlorophonia Prong-billedBarbet of tropicalforests and in some temperateforests PaltryTyrannulet HouseWren 1985, Gentryand Dodson 1987) and CommonBush-Tanager (Nadkamrni vary among forest types with respect to species Basedon <10 foragingobservations. richness, structure,and other community char- acteristics.In which foresttypes might we expect on the invertebratesin suspendeddead leaf clus- epiphytesto have a stronginfluence on birdcom- ters of South American forests. They proposed munityecology? The epiphytesin temperaterain that this resource,which occurson a year-round forests that are comparable in biomass to the basis almost exclusively in tropical forests, en- epiphytesof tropicalmontane forests (Nadkarnmi hances both the resourcebase of the forest and 1985) consist exclusively of nonvascular and the potentialfor specialization,which would in- lower vascular plants, and thus do not provide flowerand fruitresources used crease species diversity. The pool of epiphyte the rich frequent- We resourcesand the degree of preferentialuse we ly by frugivorousand nectarivorousbirds. could find no data on insectivorousbird use of describefor a Costa Rican landscapemay func- in humus of tem- tion in the same way. invertebratesliving canopy peratewet forests. MECHANISM2: TEMPORAL Epiphytesare found in nearly all tropical for- PARTITIONINGOF RESOURCES ests, but their composition and biomass varies Many tropical forests are subject to major sea- greatly among habitats. The most striking dis- sonal fluctuations in production of food re- tributionalpattern of epiphytesis a dramaticde- sources, and some frugivores switch to other crease in the number of epiphyte species and "keystone plant resources"such as flowers, fo- individualsin dry habitats(Gentry and Dodson liage,and sapwhen fruits are rare (Terborgh 1986, 1987). Even in the driest habitats, however, or- Terborghand Stern 1987). Althoughthese foods chids, cacti, bromeliads,and ferns can be found may be of poor nutritionalquality, they are im- and may provide importantarboreal resources, portantto the frugivorecommunity, because they especially when their deciduous host trees are tide the animals over an otherwiseunfavorable leafless. Lowland wet tropical forests are ex- time of year. Althoughfew quantitativedata on tremely rich in terms of epiphyte diversity, and epiphytephenology at the communitylevel exist, are dominated by hemi-epiphytes,aroids, bro- some epiphytesdiffer in phenologycompared to meliads, and woody shrubs.However, they tend host trees (Croat 1975, Feinsingeret al. 1987). to lack the contiguous moss mats of montane During our field study period, only seven of the foreststhat fosteraccumulations of dead organic

This content downloaded from 128.171.57.189 on Mon, 13 May 2013 21:28:23 PM All use subject to JSTOR Terms and Conditions BIRD USE OF EPIPHYTES 899 matter (Gentry and Dodson 1987). In contrast, GeographicSociety Committee on Researchand Ex- tropical elfin forest trees are covered with large ploration,the Whitehall Foundation, and the National The loads of cryptogamsand associated crown hu- ScienceFoundation (BSR 86-14935). Tropical Science Center facilitatedlogistics in Costa Rica. We mus, but lack the angiospermcomponent that thankG. Keysand S. Perkinsfor helpin the field.J. would provide a large resource base for frugi- Campbell,T. Guindon,W. Guindon,O. Leiton,and vorousand nectarivorousbirds. Neotropical mid- othermembers of the Monteverdecommunity kindly elevation forests (2,000-2,500 m in the Andes providedaccess to our researchsites. J. Longino,S. Rothstein,C. D'Antonio,M. Lawton,R. Pierotti,L. and 1,800-2,100 m in CentralAmerica) support Hunt,T. McLellan,and A. Kurisgave editorial help. the greatesttaxonomic and structuraldiversity J.V. Remsenand B. Loiselle provided extensive advice of epiphytes of any forest type (Madison 1977), on the literaturereview and on our interpretationof and the epiphyte community in those habitats the data. would most enhance bird strongly diversity. LITERATURE CITED If structuraldiversity and new resources are importantcomponents of increasedbird diver- ABENDROTH,A. 1965. Bromeliadsand birds in our garden.Bromel. Soc. Bull. 15:107-108. sity in the tropics,then species diversity of birds AMERICAN UNION. 1983. Check- using epiphytes(percent use, specialization,etc.) list of NorthO1crrHoLooxsS' American birds. 6th ed. American should increase along the same gradientsof in- Ornithologists'Union, Washington,DC. creasedepiphytic plant diversity in tropical for- AMUCHASTEGUI,A., AND H. SICK. 1967. Studies of ests. In fact, some data Orians and birdsand mammalsof SouthAmerica. D. Van by (1969) NJ. that this Nostrand,Princeton, Terborgh(1975) suggest might be true. BENZING,D. H. 1987. Vascular epiphytism: taxo- The available information on bird-epiphytere- nomic participationand adaptivediversity. Ann. lationshipsindicates the potentialimportance of MO Bot. Gard. 74:183-204. epiphytes to certain tropical birds, but deter- CODY,M. L. 1974. Competitionand the structure of mination of how influencethe avifauna as birdcommunities. Monogr. Popul. Biol. 7. Prince- they ton Univ. Press, Princeton,NJ. a whole awaits furtherinvestigation. Quantita- CROAT,T. B. 1975. Phenologicalbehavior of habit tive informationis needed on the relative nutri- and habitatclasses on BarroColorado Island (Pan- tional and energyvalues ofepiphyte vs. host tree ama CanalZone). Biotropica7:270-277. resources,the quantities and phenology of epi- CRUZ,A. 1978. Adaptive evolution in the Jamaican BlackbirdNesopsar nigerrimus.Ornis Scand. 9: phyticresources available to birdsrelative to host 130-137. trees, and the abundanceand availability of in- DAVIDAR,P. 1983. Birdsand neotropicalmistletoes: vertebratesdwelling in epiphyte-createdmicro- effects on seedling recruitment.Oecologia (Berl.) habitats.Time-based studies focusingon the be- 60:271-273. havior of birds will be crucial to determine the ELEY, J. W., G. R. GRAVES,T. A. PARKER, III, ANDD. R. HUNTER.1979. Notes on Siptornisstriaticollis importance of epiphytes to birds. Because our (Furnariidae)in Peru. Condor 81:319. field season coincided with the North American FEINSINGER,P. 1977. Notes on the hummingbirds of summer,epiphyte use by temperatemigrants re- Monteverde, Cordillerade Tilaran, Costa Rica. mains unknown. Wilson Bull. 89:159-164. Researchers these should FEINSINGER,P., J. BEACH, Y. LINHART, W. BUSBY, AND addressing questions K. MURRAY.1987. Disturbance,pollinator pre- note that gatheringinformation from observa- dictability,and pollination success among Costa tion positions within the canopy greatly en- Rican cloud forestplants. Ecology 68:1294-1305. hanced our ability to discriminatebetween the FITZPATRICK,J. W. 1980. Foragingbehavior of Neo- sourcesand types of resourcesused by birds.The tropicaltyrant flycatchers. Condor 82:43-57. FRAGA,R. 1984a. Aspectos de la biologia reprod- degree of specializationon resourceswithin the uctivadel PicaflorVerde Comun. Hornero 12:156- canopy and even on single plants (as in the case 158. of Norantea) would be impossible to discern if FRAGA,R. 1984b. Notes sobres la conductay nidi- observations were made from the ground. As ficacion de la mosquetaMyophobus fasciatus en Buenos Aires, Argentina. canopy equipment becomes more widely used, Hornero 12:96-106. GENTRY, A. H., AND C. H. DODSON. 1987. Diversity more questions concerning the interactions of and biogeographyof neotropical vascular epi- canopy plants and animals can be addressed. phytes. Ann. MO Bot. Gard. 74:205-233. GREENBERG,R. 1981. The abundance and seasonality ACKNOWLEDGMENTS of forestcanopy birds on BarrowColorado Island, Panama.Biotropica 13:241-251. This researchwas supportedby grantsfrom the Uni- JENIK, J. 1973. Root systemsof tropicaltrees. 8. Stilt- versity of CaliforniaAcademic Senate, the National and allied adaptations.Preslia 45:250-264.

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This content downloaded from 128.171.57.189 on Mon, 13 May 2013 21:28:23 PM All use subject to JSTOR Terms and Conditions APPENDIX 1. Bird use of epiphytes, compiled from 55 published studies. resource Fl = = = Epiphyte type: Flowers (mainly nectar);Fo General foraging;Fr 0, Fruits;In = Invertebrates;Ne = Nesting material,nest sites, or nest cover; Se = seeds;Un = Unknown;Wa = Water.Epiphyte taxon: Ar = Aroids;B = Bromeliads; Be = Begoniaceae;C = Clusiaspp.; E = Ericaceousshrubs; F = ferns;G = Generalepiphyte mats, encompassinga variety of unidentifiedspecies; Gu = Guttiferae; z Ma = Marcgraviaceae; Mi = mistletoes; Mo = mosses and bryophytes; O = Orchidaceae; R = Rubiaceae; So = Solanaceae; Un = Unknown.

Birdfamily Genus Species Resource Epiphytetaxon Source z, Accipitridae Spizaetus ornatus Ne B 14 unicolor Se Ar 12 Columbidae Columba fasciata Fr Mi 38 Columba flavirostris Fr, Ne Mi, U 38 Columba nigrirostris Fr Mi 13 Cuculidae Piaya cayana Ne B 38 Trochilidae Doryfera ludoviciae Fl, Ne B, E 55 Glaucis hirsuta Fl B, Ma 42 Phaethornis guy Fl B, E, G, Ma, R 42, 55 Phaethornis superciliosus Un G 50 H3 Phaethornis eurynome Fl B 1 Phaethornis longuemareus(adolphi) Fl B 42 Campylopterus curvipennis Fl B 50 Eupetomena macroura Fl B 1 Hl Florisuga mellivora Fl Ma 42 Colibri delphinae Fl E, G, Gu, Ma 55 (# Colibri thalassinus Fl B, E, Mi, Un 39, 55 03 Anthracothorax nigricollis Fl Ma 42 z Anthracothorax mango Fl B 9 Abeillia abellei In Mo 51 Popelairia conversii Fl Gu, Ma 55 Chlorestes notatus Fl Ma 42 Chlorostilbon aureoventris Ne B 8 Thalurania colombica Fl 0 37 Panterpe insignis Fl, Fo, Un B, E, Mi, Un 5, 15, 39, 46, 5 Trochilius polytmus Fl B, G, Ma 9 Leucochloris albicollis Fl B 1 Amazilia candida Fl B, Mi 50 Amazilia chionopectus Fl B, Ma 42 Amazilia cyanifrons Fl B 43 Amazilia tobaci Fl B, Ma 42 Amazilia yucatanensis Fl B 50 Amazilia tzacatl Fl, Wa, Un B, Ma, Mo, So 32, 37, 50 Eupherusa nigriventris Fl B, E, G, Gu, Ma, O 55 Elvira cupreiceps Fl B, E, Gu, Ma, O 55 Lampornis amethystinus In Mo 51 Lampornis hemileucus Fl B, E, G, Gu, Ma, O 55

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Birdfamrily Genus Species Resource Epiphytetaxon Source Lampornis castaneoventris Fl B, E, G 55 Heliodoxa jacula Fl B, E, Ma 55 Eugenes fulgens Fl B, E 55 Coeligena prunellei Fl B 43 Mellisuga minima Fl B 9 Selasphorus flammula Fl B, E, Mi 55 Non-hermit Fl B, G, E 45 Hermit Fl B, G, E 45 Trogonidae Trogon aurantiiventris Fr, Ne E, Un 38, 54 Trogon violaceus Ne Un 37 Capitonidae Capito maculicoronatus Ne Mo 34 Semnornis frantzii Fr, Ne Ar, Ma, U 36, 38 Ramphastidae Aulacorhynchus prasinus Fr, Ne, Se Ar, Ma, So 12, 36, 38, 54 Petroglossus frantzii Fr Ma 36 Picidae Melanerpes radiolatus Fo Un 9 Melanerpes rubricapillus Fr Ma 36 Centurus pucherani Fo, Wa Mo, Un 39 Piculus rubiginosus Fo Mo 39 Piculus rivolii Fo Mo 29 Piculus simples Fo Un 37 Dendrocolaptidae Dendrocincla homochroa Fo Mo 39 Xiphorhynchus guttatus In Mo, So 37 Lepidocolaptes affinis Fo Mo 29 Furnariidae Snynallaxis gularis Fo Mo 23 Cranioleuca erythrops Fo, In Un 25, 39 Cranioleuca vulpina In Un 26 Cranioleuca marcapatae Fo Mo, B 20 0 Cranioleuca albiceps Fo Mo 29 Cranioleuca albicapilla Fo Mo, B 20 Schizoeaca harterti Fo Mo 29 Asthenes urubambensis Fo, In Mo 20 Siptornis striaticollis Fo Mo 5 •T Margarornis bellulus Fo B, Mo 31 Premnoplex brunnescens Fo, In Mo, Un 27, 39 ,...0o Pseudocolaptes lawrencii Fo Un 30 Pseudocolaptes boissonneautii Fo Mo, Un 20 or Syndactyla subalaris In Un 25 Automolus ruficollis Fo B, F, Mo 23 Thripadectes rufobrunneus Fo Un 39

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Birdfamily Genus Species Resource Epiphytetaxon Source Formicariidae Cymbilaimus lineatus Ne F 34 Dysithamnus striaticeps Ne Mo 34 z Cotingidae Zaratornis stresemanni Fr Mi 19 Pipreola riefferii Ne Mo 16 Pachyramphus versicolor Ne Mo 34 Pipridae Pipra coronata Fr Ma 36 Chiroxiphia linearis Fr G 54 z Manacus vitellinus Fr Mi 13 Tyranneutes stolzmanni Fr Un 24 Piprites chloris Fr Un 24 fZ Tyrannidae Myiotheretes fumigatus Fo, In Mo, Un 20 similis Fr Mi 13 Myiozetetes H Attila spadiceus Ne B, Be, Un 37 Contopus lugubris Ne Mo 34 Empidonax flavescens Ne Mo 34 Mitrephanes phaeocercus Ne Mo 34 Myiopagis flavivertex Fr Mi 9 Lophotriccus pileatus Ne Mo 34 0 Mecocerculus stictopterus Fo Mo 29 z Elainea frantzii Ne Un 34 Myiophobus fasciatus Ne B 7 Camptostoma obsoletum Ne Mo, Un 37 Phyllomyias uropygialis Fo Mo 29 Zimmerius vilissimus Fr Mi 13 Zimmerius bolivianus Fo Mi 30 Tyranniscus elatus Fr Mi 13 Mionectes olivaceus Fr Mi 54 Mionectes oleagineus Fr Mi 13 Oxyruncidae Oxyruncus cristatus(frater) Fo, Fr, In E, Mi, Mo, Un 39, 48 Corvidae Cyanocitta stelleri Fo Mo 34 Cyanolyca pumilo Fo Un 34 Psilorhinus morio Wa B 11 Troglodytidae Odontorchilus branickii Fo Mo 22 Troglodytes ochraceus Fo, In Un 25, 39 Troglodytes solstitialis Fo Mo 29 Henicorhina leucophrys In Un 26 Turdidae Myadestes melanops Fr, Ne E, G, Ma, Mo, So 34, 54 Myadestes obscurus Ne 0 34 Myadestes ralloides Ne Mo 16

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Birdfamily Genus Species Resource Epiphytetaxon Source Turdus serranus Ne Mo 16 Turdus plebejus Fo, Fr, Ne, Se At, Ma, Un 12, 34, 54 Turdus ignobilis Ne Mo 16 Turdus grayi Ne, Se B, Gu, Ma, Mi, Un 17, 36, 37 Ptilogonatidae Ptilogonys cinereus Fr, Ne Mi, Mo, So 18, 33, 49 Ptilogonys caudatus Fo, Ne Mi, So 33 Phainoptila melanoxantha Se Ar 12 Phainopepla nitens Fr Mi 52 Vireonidae Cyclarhis gujanensis Ne E 34 Parulidae Mniotilta varia In B 10 Vermivora gutturalis Ne B 34 Dendroica pharetra In B 10 Dendroica dominica In B 10 Dendroica tigrina In B 10 Helmitheros vermivorus In B 10 Myioborus miniatus Ne Mo 16 Myioborus melanocephalus Fo Mo 29 Icteridae Psarocolius wagleri Fo Mo, Un 48 Cacicus uropygialis Fo, In, Ne Mo, Un 34, 36, 48 Cacicus leucorhamphus Fo, In Mo 29 Icterus leucopteryx Fo Un 9 Nesopsar nigerrimus In B, Mo, Un 3, 9 Thraupidae Dacnis cayana Fr Ma, Mi 36, 41 Chlorophanes spiza Fl, Fr, In, Wa B, Gu, Ma, Mi, So 36, 37, 41 Cyanerpes lucidus Fo, Fr, Ne Ma, Un 34, 36 Cyanerpes caeruleus Fr Mi 41 C: Cyanerpes cyaneus Fr Ma 36 Diglossa cyanea Fo Un 29 Diglossa plumbea Fl, Fo E, Un 39, 55 Euneornis campestris Fl B, G 9 Conirostrum sitticolor Fo Un 29 mT Coereba flaveola Fr C, Mi 41 Chlorornis riefferii Fo Mo 29 Chlorospingus ophthalmicus Fr, In, Ne, Se Ar, E, G, Mo, Un 12, 26, 34, 54 Chlorospingus inornatus Fo Mo 31 0 Chlorospingus pileatus Se Ar 12 Chlorospingus canigularis Fo Mo 21 Hemispingus calophrys Fo Mo 29 Heterospingus rubrifrons Fr Mi 13 Tachyphonus luctuosus Fr Ar 41

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Birdfamily Genus Species Resource Epiphytetaxon Source 0 Tachyphonus rufus Fr Ar, B, Mi 41 Piranga bidentata Ne Un 34 Calochaetes coccineus Fo Mo 21

Ramphocelus carbo Fr Ar, B 41 o\ Ramphocelus passerinii Fr Ma, So 36, 37 Thraupis episcopus(virens) Fo Ma 36 Thraupis palmarum Fr C, Ma 36, 41 Buthraupis montana Fo Mo 29 Dubusia castaneoventris Fo, In Mo, B 20, 28, 29 tj Euphonia jamaica Fr, Ne B, Mi 9 Euphonia affinis Fr Mi 39, 49 Euphonia luteicapilla Fr Mi 39 Euphonia violacea Fr Ar, B, C, Mi 41 Euphonia laniirostris Fr Mi 39 Euphonia hirundinacea(lauta) Fr Mi 39, 49, 54 Euphonia elegantissima Fr Mi 16, 39, 49, 53 Euphonia imitans Fo, Fr, Ne F, Ma, So, Un 36 Euphonia gouldi Fr Mi 39 'r~l Euphonia minuta Fo, Fr Mi, Mo 34 zj Euphonia rufiventris Fr Un 24 Chlorophonia callophrys Fr Ma, Mi, So 54 Tangara inornata Fr Mi 13 C Tangara mexicana Fr C, Mi 41 Tangara chilensis Fr Mi 2 Tangara icterocephala Fo, Fr, In, Ne Gu, Ma, Mo, So 36, 37, 39 Tangara chrysotis Fo Mo 21, 28 Tangara guttata Fr Ma 36 Tangara gyrola Fr Ma, Mi 36, 41 Tangara larvata Fr, In, Se Gu, Ma, Mi, Mo, So 13, 36, 37 Tangara vassorii Fo Mo 29 Tangara callophrys Fo Mo 39 Tangara fucosa Fo Mo, Un 31 Emberiadae Loxipasser anoxanthus Fr Mi 9 Loxigilla violacea Fo, Fr G, Mi 9 Pinaroloxias inornata Fo B 40 Atlapetes rufinucha Fo Mo 29 Caryothraustes poliogaster Fr, Ne B, C, Un 34 Saltator maximus Fr Ma 36 Saltator albicollis Fr Ma 36 1. Abendroth1965. 2. Amuchasteguiand Sick 1967. 3. Cruz 1978. 4. Davidar 1983. 5. Eley et al. 1979. 6. Feinsinger1977. 7. Fraga1984a. 8. Fraga1984b. 9. Lack 1976. 10. Lackand Lack 1972. 11. M. F. Lawton1983. 12. R. O. Lawton 1983. 13. Leck 1972. 14. Lyon and Kuhnigk 1985. 15. McWilliams1974. 16. Miller 1963. 17. Morton 1983. 18. Newman 1950. 19. Parker1981. 20. Parkerand O'Neill 1980. 21. Parkerand Parker1982. 22. Parkeret al. 1980. 23. Parkeret al. 1985. 24. Pearson1977. 25. Powell 1979. 26. Powell 1980. 27. Powell 1983. 28. Remsen 1984. 29. Remsen 1985. 30. Remsenand Parker1983. 31. Robbinset al. 1985. 32. Skutch1931. 33. Skutch1965. 34. Skutch1967. 35. Skutch1972. 36. Skutch 1980. 37. Skutch1981. 38. Skutch 1983. 39. Slud 1964. 40. Slud 1967. 41. Snow and Snow 1971. 42. Snow and Snow 1972. 43. Snow and Snow 1980. 44. Snow 1981. 45. Stiles 1978. 46. Stiles 1983. 47. Stiles 1985. 48. Stiles and Whitney 1983. 49. Sutton 1951. 50. Toledo 1975. 51. Wagner 1946. 52. Walsberg1975. 53. Wetmore1914. 54. Wheelwrightet al. 1984. 55. Wolfet al. 1976.

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APPENDIX 2. Birds seen in study sites that did not use epiphytes.

Family Scientificname Commonname Cathartidae Cathartesaura TurkeyVulture Coragypsatratus BlackVulture Accipitridae Elanoidesforficatus Swallow-tailedKite Falconidae Micrasturruficollis BarredForest-Falcon Cracidae Chamaepetesunicolor Black Columbidae Columbafasciata Band-tailedPigeon Columbasubvinacea Ruddy Pigeon Leptotilaverreauxi White-tippedDove Psittacidae Pionopsittahaematotis Brown-hoodedParrot Cuculidae Piaya cayana SquirrelCuckoo Crotophagasulcirostris Groove-billedAni Apodidae Streptoprocnezonaris White-collaredSwift Chaeturavauxi Vaux's Swift Trochilidae Phaethornisguy Green Hermit Amazilia saucerottei Steely-ventedHummingbird Trogonidae Pharomachrusmocinno ResplendentQuetzal Trogonaurantiiventris Orange-belliedTrogon Momotidae Momotus momota Blue-crownedMotmot Picidae Melanerpeshoffmanni Hoffmann'sWoodpecker Piculus rubiginosus Golden-oliveWoodpecker Dryocopuslineatus LineatedWoodpecker Campephilusguatemalensis Pale-billedWoodpecker Dendrocolaptidae Sittasomusgriseicapillus OlivaceousWoodpecker Xiphocolaptespromeropirhynchus Strong-billedWoodcreeper Xiphorhynchuserythropygius SpottedWoodcreeper Furnariidae Cranioleucaerythrops Red-facedSpinetail Thripadectesrufobrunneus Streak-breastedTreehunter Cotingidae Tityrasemifasciata MaskedTityra Tyrannidae Tyrannusmelancholicus TropicalKingbird Myiodynastesluteiventris Sulphur-belliedFlycatcher Myiodynastesmaculatus StreakedFlycatcher Myiozetetessimilis Social Flycatcher Attila spadiceus Bright-rumpedAttila Elaenia chiriquensis LesserElaenia Rhynchocyclusbrevirostris Eye-ringedFlatbill Hirundinidae Notiochelidoncyanoleuca Blue-and-whiteSwallow Corvidae Cyanolycacucullata Azure-hoodedJay Troglodytidae Henicorhinaleucophrys Gray-breastedWood-Wren Turdidae Turdusgrayi Clay-coloredRobin Vireonidae Hylophilusdecurtatus LesserGreenlet Parulidae Dendroicafusca BlackburnianWarbler Basileuterusculicivorus Golden-crownedWarbler Icteridae Sturnellamagna EasternMeadowlark Thraupidae Pirangaflava HepaticTanager Thraupisepiscopus Blue-grayTanager Euphonia anneae Tawny-cappedEuphonia Tangaradowii Spangle-cheekedTanager Fringillidae Zonotrichiacapensis Rufous-collaredSparrow Tiarisolivacea Yellow-facedGrassquit

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