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BIOTROPICA 35(4): 520529 2003

Capture Rates of Male Euglossine Bees across a HumanIntervention Gradient, Choco Region, Colombia1

J. Tupac Otero2,3

Departamento de Biologa, Universidad del Valle, A.A. 25360, Cali, Colombia

and

Juan Carlos Sandino 4

Fundacion Herencia Verde, A.A. 38302, Cali, Colombia

ABSTRACT

Euglossine bees are important pollinators of lowland Neotropical forests. Compared to disturbed habitats, undisturbedones have been previously characterized by higher abundance and diversity of euglossine bees. Most past studies haverelied on chemically baiting male bees at single sites within habitats. Over a two-year period, we employed a repeated-measures design in which we sampled bees at multiple sites within three different habitat types, reflecting a mosaicof human disturbance (farm, secondary forest, and old logged forest). After 22 monthly samples, a total of 2008 male

bees were captured, representing 31 species in five genera: 1156 at the farm (57.6%, 21 spp.), 505 in the secondaryforest (25.1%, 27 spp.), and 347 in the old logged forest (17.2%, 21 spp.). Eighty-one percent of the bees capturedbelonged to the five most abundant species: Eulaema cingulata, El. chocoana, Euglossa hansoni, Eg. ignita, and Eg.imperialis. These species differed significantly in capture frequencies among habitats. Eulaema cingulata, El. chocoana,and Eg. ignita were captured most frequently at the farm, while Eg. imperialis was most abundant in the secondaryforest. In contrast, Eg. hansoni, the sole short-tongued species among the five, was equally abundant in the two foresthabitats but occurred rarely on the farm. Additionally, habitats differed in bee composition. The high capture ratesfor long-proboscis species at the farm may have been due to their ability to extract nectar from flowers with longfloral tubes, which probably occurred at a greater density on the farmed land than in the adjacent forests.

RESUMEN

Las abejas euglosinas son polinizadores importantes en bosques neotropicales de tierras bajas. Normalmente, los habitats

poco perturbados se caracterizan por presentar una mayor abundancia de abejas euglosinas que los menos intervenidos,aunque dichos resultados se basan en muestreos que usan atrayentes qu micos para machos en sitios unicos por habitat.En este estudio realizamos muestreos basados en sitios multiples en tres habitats adyacentes (finca, bosque secundario,y bosque maduro) a lo largo de dos anos. Encontramos una mayor abundancia y diversidad de machos euglosinos enlos habitats con mayor perturbacion humana que en el bosque maduro. Despues de 22 muestreos mensuales captu-ramos un total de 2008 abejas representando 31 especies en cinco generos: 1156 en la finca (57.6%, 21 spp), 505en el bosque secundario (25.1%, 27 spp), y 347 en el bosque maduro (17.2%, 21 spp). El 80.8 por ciento de lasabejas capturadas pertenecan a las cinco especies mas abundantes: Eulaema cingulata, El. chocoana, Euglossa hansoni,Eg. ignita, y Eg. imperialis. Para estas especies encontramos diferencias en la frecuencia de captura entre habitats.Eulaema cingulata, El. chocoana, y Eg. ignita fueron mas frecuentes en la finca, mientras que Eg. hansoni, la unica delas cinco con lengua corta, lo fue en los dos habitats boscosos y Eg. imperialisen el bosque secundario. Adicionalmente,los habitats difirieron en composicion de abejas. Lo resultados pueden deberse a que en la finca haba una mayoroferta de nectar con acceso restringido que en los busques adyacentes. El nectar, por estar en flores de corolas profundas,solo poda ser accedido por abejas de lenguas largas lo cual favoreca una mayor abundancia de euglosinas grandes

con lenguas largas en la finca que en los bosques adyacentes.

Key words: Choco; Colombia; Euglossa; euglossine bees; Eulaema; human intervention gradient; pollinators.

EUGLOSSINE BEES (EUGLOSSINI, APIDAE) ARE AMONGthe most important long-distance pollinators of

1 Received 18 November 2002; revision accepted 27 Au-gust 2003.2 Corresponding author; e-mail: [email protected] Current address: CSIRO Plant Industry, Australian Na-

tional Herbarium, GPO Box 1600, Canberra, ACT2601, Australia.4 Current address: Facultad de Biologa Marina, Universidad

Jorge Tadeo Lozano, Carrera 22-61, Bogota, Colombia.

lowland Neotropical forests (Bawa 1990). The ca200 species of this group (Kimsey & Dressler1986) pollinate a vast array of plants at all succes-sional stages (Gilbert 1980, Dressler 1982a, Acker-man 1985). The taxonomy, ecology, and naturalhistory of euglossine bees are well documented(Zucchi et al. 1969, Ackerman et al. 1982, Dressler1982a, Janzen et al. 1982, Williams 1982, Roubik& Ackerman 1987, Roubik 1989, Bonilla & Nates1992, Armbruster 1993, Fernandez 1995). Theirmost remarkable feature is the fragrance-foraging


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Euglossines across an Intervention Gradient 521

activity of males at flowers of several different plantfamilies and non-floral sources such as rotting logs(Williams 1982, Whitten et al. 1993). The role ofeuglossine bees as long-distance pollinators is crit-ical because many plant species require cross-pol-

lination (Bawa 1990, Kress & Beach 1992, Oyama1993) but exist at very low population densities(Faber-Langendoen & Gentry 1991, Clark 1992).Some authors have hypothesized that patches ofabundant resources resulting from deforestationand farming practices may disrupt the foraging dy-namics of euglossine bees in adjacent forests, andthus the gene flow they mediate as pollinators maybe severely affected (Janzen 1974, Aldrich & Ham-rick 1998).

Since identifying the main components of the

attractive fragrances, commercially available chem-icals have been used for obtaining, in a few days,large samples of euglossine communities at givenlocalities (Janzen et al. 1982, Ackerman 1983,Pearson & Dressler 1985, Powell & Powell 1987,Roubik & Ackerman 1987, Sandino 1995a). Mostsuch samplings have been done at single locations

within habitats and at single habitats within land-scapes. Capture rates are assumed to reflect actualbee abundance at each habitat (Roubik 2001). Be-cause foraging for nectar and fragrances and sexualdisplays may each be performed at different and

distant sites (Janzen et al. 1982), we can assumethat capture rates reflect the use that males makeof each habitat. Some evidence supports this as-sumption. Male euglossine bees may be collectedin higher frequency near the sites from which theyobtain food or fragrances (Ackerman 1983, Arm-bruster 1993). Because they do not collect fra-grances everyday, but do feed frequently, it seemslogical to suppose nectar distribution as a main, butnot sole, causal factor of the capture frequencies.

And because euglossine bees probably forage across

ample distances between patches (Janzen 1971,1981), and given evidence of between-site variabil-ity in baitcapture samples from a single habitat(Ackerman 1983, Armbruster 1993; cf. Roubik2001), euglossine foraging and demographic dy-namics may be better addressed by long-term sam-pling and multiple-habitat and multiple-site sam-pling.

Previous studies on the effects of deforestationand fragmentation on euglossine bee communitieshave been incomplete (Cane 2001) and based onsingle-site sampling (Powell & Powell 1987, Becker

et al. 1991). The main objective of our study wasto document the differences in euglossine bee com-munity structure through a human intervention

gradient at a lowland site in the Choco biogeo-graphic region of Colombia. To accomplish thisgoal, we employed a repeated-measures design in

which, over a two-year period, we followed specificsampling plots in three habitat types reflecting dif-

ferent levels of human disturbance. Specifically, weasked: (1) Are euglossine bees more abundant anddiverse in forested habitats than in a farm?; (2) Docapture rates differ among sites within habitats?; (3)Do forested and farm sites differ in euglossine beecomposition?; (4) What bee characteristics may berelated to capture rates among the sampled habi-tats?; and (5) Do capture rates vary across years?

METHODS

STUDY SITE

. This study was conducted in the cen-tral Pacific plain of Colombia by the old Cali-Bue-naventura road (completed in 1946, but now sel-domly used), which is near the town of Guaima(346N, 7657 W) on the Anchicaya River. Thearea, part of the biogeographical region of Choco,receives more than 7000 mm of annual rainfall andhas an average relative humidity of 96 percent.Study sites were between 50 and 80 m elevation,ranging from the riverbanks to low hills. The forestis classified in the Holdridge system as transitionalbetween tropical wet and tropical pluvial forest

(IGAC 1977).Indigenous peoples first settled in this zone at

least 2200 years ago (Herrera 1989) and were re-placed by AfroAmerican communities that fol-lowed similar farming practices. The present hu-man community and landscape have resulted fromthe merging of traditional self-sufficient commu-nities of farmers and miners with more recent col-onizers. The present AfroColombian communitydepends mainly on a subsistence economy basedon timber extraction, mining, agriculture, fishing,

and hunting. Farmlands are present all along the Anchicaya River, and secondary forests abut thefarms and roads.

Based on their accessibility, we chose three dif-ferent habitats that represented the most commonhabitat gradients within the landscape (Tables 1and 2). These habitats were a traditional farm (Fa),a selectively and intensively logged secondary forest(SFo), and a less disturbed old logged forest (OFo).The farm, named Limones and property of thecommunity organization AFEPAL, was a multi-crop farm having several cultivars that included

both food and timber products (Table 1). It was80 ha on the west margin of the Anchicaya Riverand adjacent to secondary forests. The secondary


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522 Otero and Sandino

TABLE 1. Plant species at the study sites (R. Ospina, pers. comm.).

Site Plant species

Farm Cultivars: Chontaduro (Bactris sp.), green plantain (Musa paradisiaca), cassava (Mani-hot esculenta), breadfruit (Artocarpus altilis), sugarcane (Saccharum officinale), and

borojo (Borojoa patinoi)Dominant trees: Cedrela odorata (Meliaceae) and Cecropiaspp. (Cecropiaceae)Herbs reported as euglossine resources: Calathea spp., Heliconia spp., and Anthurium

spp.Secondary forest Dominant trees: Mabea sp. (Euphorbiaceae), Cespedesia spatulata (Ochnaceae), Otoba

latialata(Myristicaeae), Miconia spp. (Melastomataceae), Wetinia quinara (Areca-ceae), Chrysophillumsp. (Sapotaceae), Brosium utile (Moraceae)

Herbs reported as euglossine resources: Anthurium spp.Old logged forest Dominant trees: Dussia lehemani (Fabaceae), Socratea exorrhiza (Arecaceae), Licania

duriflora (Chrysobalanaceae), Cecropiasp. (Cecropiaceae), Brosium utile (Moraceae),and Symphonia globulifera (Clusiaceae)

Herbs reported as euglossine resources: Anthurium sp. and other plant species

TABLE 2. Structural measurements of the study sites (means SD).

SiteCanopy height

m (SD)

Trees 10 cmDBH/ha

no. (SD)Average DBH

cm (SD)

FarmSecondary forestOld logged forest

12.4 (6.2)13.2 (4.4)20.7 (6.5)

5875 (3025)19,925 (4225)

7625 (1625)

50.1 (56.7)27.3 (21.1)44.4 (39.2)

forest had constant human intervention for timberextraction and hunting by local people. The oldlogged forest had intense commercial timber ex-traction from the 1940s until ca 15 years beforeour study, although selective timber extractionalong the Yesqueros stream was still frequent forlocal uses. The old logged forest, however, was con-tinuous with a natural undisturbed forest that ispart of the Buenaventura municipal reserve of SanCipriano. In each habitat, we established four sam-pling sites (Fa 14, SFo 58, and OFo 912) lo-

cated at least 200 m away from each other, inagreement with Armbrusters (1993) heterogeneousresults between sites.

H ABITAT STRUCTURE. At each of four samplingsites per habitat, we estimated the canopy heightusing a clinometer, the average diameter of trees atbreast height (DBH), and the tree density as thenumber of trees larger than 10 cm DBH within a40 40 m plot. During the last months of ourstudy, a floristic profile was determined by otherresearchers along our sampling routes. Their spec-imens were deposited at the Herbarium of the Uni-versidad del Valle (CUVC).

BEE SAMPLING DESIGN. At each sampling site, weplaced three homemade, nonlethal traps (Sandino

in press) made from plastic dispensable bottles andnylon stockings attached to the top in which thebees arrived looking for the fragrance and wereadded to a vial. The bees were able to enter thetrap to collect the fragrance, but once inside weretrapped in the stockings when attempting to leave(Sandino 1995a). We used three different chemicalbaits, one per trap at each site: 1-8 cineole, methylsalycilate, and skatole. Bees were active between0730 and 1430 h (Sandino, pers. obs.). Traps wereopened from 0800 until 1200 h and checked every

30 minutes. The three habitats were sampled si-multaneously by three different collectors. Samples were collected every four weeks, when possible,from 25 June 1995 to 28 July 1997.

Bees captured were identified in the field usinga guide based on a previous reference collectionfrom the same locality and also by consulting spec-imens available from other studies in the Chocoregion (Sandino 1995b) and elsewhere in Colom-bia (Bonilla & Nates 1992). If a bee could not beidentified in the field, it was collected. Voucherspecimens were deposited in the bee laboratory atthe Universidad Nacional, Bogota, Colombia, and

were identified using keys from the literature(Dressler 1978a, b, 1979, 1982b; Kimsey 1982;Bonilla & Nates 1992; Ospina 1998) and by com-parison with bees deposited there. Once identified,


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bees were marked on a wing using an indelible inkmarker (Outliner, Sakura, Hayward, California)

with a color specific to each habitat and then setfree. In marking bees, our goal was to estimate re-capture frequencies to assess the independence of

our sampling regime as well as to estimate popu-lation sizes if recaptures were high.

MORPHOMETRIC RANKS OF THE BEES. Even folded,the proboscis is notably long in many euglossinespecies (thus the name for the taxon), in some casesexceeding body length. Species with short-foldedprobosces are generally those Euglossain which theproboscis does not reach the abdomen. Euglossabees are more like honeybees in size, while Eufrieseaand Eulaema are more bumblebee-like. Thus, we

grouped the vouchers according to the above dis-tictions. Because wing length is linearly correlated with body size (Kimsey 1982) and tongue mea-surements vary 210 percent (Roubik 1992) withinspecies, we used the folded proboscis length andthe anterior wing length of bees to classify eachspecies in one of three morphometric classes: largebees, with wings larger than 1.2 cm and foldedproboscis longer than 0.8 cm; medium-sized, long-tongued bees, with wings shorter than 1.2 cm andfolded proboscis longer than 0.8 cm; and medium-sized, short-tongued bees, with wings shorter than

1.2 and folded proboscis shorter than 0.8 cm.

DATA ANALYSIS. To test for differentiation in hab-itat structure, we performed a KruskalWallis test(KW) on the canopy height and the tree densitydata. With the 22 samples of bees, we created fre-quency tables for each of the 12 sites (264 cases).

We tested bee frequency distribution for normality,using the AndersonDarling test. We calculated theabundance, richness, the ShannonWiener diver-sity index (H), and the evenness (J) according to

Zar (1999), and the Simpsons index of dominance(li) that measures the probability of randomly se-lecting two individuals of the same species in acommunity (Brower et al. 1997).

To test if species richness and abundance ofbees were equal across all habitats, we performedrepeated measures ANOVA (Zar 1999) on the nat-ural log transformed data for number of bees andthe number of bee species. We repeated these anal-yses using abundance data from the five mostabundant species, because those corresponded to80.8 percent of the captures. Using the repeated

measures ANOVA design, we tested for differencesamong sites within habitats (subject effects), differ-ences among habitat types (treatment effects), and

the interaction between habitat type and time. Be-cause we sampled over two years, our time effect(22 mo) represented seasonal effects and temporaldynamics. To determine whether or not the beecommunity changed from the first to the second

year, two principal components analyses (PCA)were conducted using a capture frequency matrixof 31 species 12 sites including the bees capturedduring both the first and second year of the study.To determine whether or not there was an overalldifferentiation in bee composition among habitats,

we performed a combined PCA with a matrix in-cluding the samples from both years. To comparethe 12 communities for year 1 versus year 2, a PCA

was done with a matrix that included samples fromeach year (June 1995June 1996 vs. July 1996

July 1997). All PCAs were performed using theprocedure PRINCOMP (SAS 1989). Finally, totest differences among habitats, we used a stepwisediscriminant analysis using the 13 most abundantspecies (PROC DISCIM; SAS 1989). Significantvariables (bee species) that remained in the model

were then used in a canonical discriminant analysis(PROC DISCIM; SAS 1989).

RESULTS

STRUCTURAL ANALYSIS OF THE HABITATS. Between

habitats, there were significant differences in treedensity (KruskalWallis, H 8.00, df 2, P0.018) and in the average DBH (H 25.12, df 2, P 0.0001) but not in canopy height (H3.58, df 2, P 0.167). At the farm, the canopyaveraged 12.4 m (SD 6.2) and tree density was23.5 (SD 12.1) per 1600 m2. The secondary for-est was the most homogeneous of the habitats interms of the DBH classes and canopy height (13.2m SD 4.4) and had the highest tree density (79.7SD 16.9 trees/1600 m2). The old logged forest

had the tallest canopy, 20.7 m (

SD 6.5), but rel-atively low tree density (30.5 SD 6.5 trees/1600m2).

BEE ABUNDANCE AND DIVERSITY. Over the 22 sam-pling dates, we collected 2008 male euglossine beesbelonging to 31 species and five genera (Table 3).No marked bees were recaptured. At the farm sites,

we captured 1156 males (57.6% of the total cap-tures) belonging to 21 species; at the secondary for-est sites, 505 males (25.1%) of 27 species; and inthe old logged forest sites, 347 males (17.2%) of

21 species. The number of captured bees was sig-nificantly different across habitats (F2, 9 33.02,P 0.0001). More bees were captured on the farm


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TABLE 3. Total captures of male euglossine bees in each of the three study habitats. Fa: farm; SFo: secondary forest; andOFo: old logged forest. The three morphometric ranks are L/L: large bees (with wings larger than 1.2 cm andproboscis longer than 0.8 cm); M/L: medium-sized with long proboscis (with wings shorter than 1.2 cm andproboscis longer than 0.8 cm); and M/S: medium-sized with short proboscis (with wings shorter than 1.2 and proboscis shorter than 0.8 cm). li: Simpsons index of dominance. H: ShannonWiener index. J: evennessindex.

SpeciesMorphometric

rank Fa SFo OFo Total

Eulaema aff. bombiformisEl. chocoanaEl. cingulataEl. sororia

L/LL/LL/LL/L

24294329

7

202738

5

23

502

46324417

14Euglossa allostictaEg. asarophoraEg. bursigeraEg. chalybeataEg. championi

M/LM/LM/LM/LM/S

27

2

12

6192

16

6828

18

399

131046

Eg. deceptrix

Eg. dressleriEg. flammeaEg. gorgonensisEg. hansoni

M/S

M/SM/LM/LM/S

4

3637

33

1

14

164

7104

103

5

117711

300Eg. ignitaEg. imperialisEg. aff. laevecinctaEg. mixtaEg. townsendi

M/LM/LM/LM/SM/S

27617

2

76107

11

10

8521

9

437145

11

21Eg. tridentataEuglossa sp. 9Glossurela sp. 1Glossurela sp. 9sp. T 21

M/SM/SM/LM/LM/L

8141714

2151

2

2

10162019

1

sp. T 23sp. Q 24Exaerete frontalisEx. smaragdina

M/LM/LL/LL/L

1

1

3

1

3

1116

Eufriesea pulchraEufrieseasp.Aglae caerulea

L/LL/LL/L

2 111

1 411

TotalBees 1156 505 347 2008Species 21 27 21 21li 0.21 0.18 0.18 0.15H 0.84 0.92 0.93 0.97

J 0.63 0.64 0.70 0.66

than in both the secondary forest and the oldlogged forest, but there were no differences be-tween the number of captures in the secondary for-est and the old logged forest (Tukey post hoc test).For three of the five most frequently collected spe-cies, there were significant differences in the num-ber of bees captured among habitats (Fig. 1): Eu-laema cingulata, (F2, 9 53.96, P 0.0001), El.chocoana (F2, 9 10.56, P 0.0043), and Eg.ignita (F2, 63 5.56, P 0.0267). The other two

species, Euglossa hansoni(F2, 9 1.69, P 0.2379)and Eg. imperialis (F2, 9 3.30, P 0.0842),showed nonsignificant differences across habitats.

These five species accounted for 80.8 percent ofthe captured males, none of which were moreabundant in the old logged forest than in otherhabitats. Eulaema chocoana, El. cingulata, and Eg.ignita were significantly more frequent at the farmthan at the other sites (X2 148.49, X2 82.32,and X2 14.02, respectively; all tests df 2, P0.005), while Eg. hansoni and Eg. imperialis werecaptured most frequently in the secondary forest(X2 266.70 and X2 109.07, respectively; both

with df 2, P 0.005). The number of speciescaptured per habitat varied significantly (F2, 9 13.78, P 0.0018). There was no significant dif-


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FIGURE 1. Number of captures for the five most com-mon species through the human intervention gradient.Fa: farm; SFo: secondary forest; and OFo: old logged for-est.

FIGURE 2. Plot of the two principal components ofthe PCA based on the proportion of bees captured at the12 sites during the (a) first year, (b) second year, and (c)combined first and second years. Sites Fa-1Fa-4 are onthe farm (Fa); Sf-5Sf-8 in the secondary forest (SFo);and Of-9Of-12 in the old logged forest (OFo).

ference in the H

index (KruskalWallis, H

1.38,df 2, P 0.50) and evenness values J (H2.28, df 2, P 0.31) for the different habitats(Table 1).

BEE COMPOSITION. The first principal componentof the overall PCA based on both years explained26 percent of the variability and separated farmand forested sites (Fig. 2c). This component waspositively correlated with the abundance ofEl. cho-coana, El. cingulata, and Eg. flammeaand negativelycorrelated with Eg. hansoni. The second principal

component explained 20 percent of the variabilityand separated secondary forest sites from old forestsites (Fig. 2c). Additionally, it separated one of thefarm sites (2) from the other three sites (1, 3, and4). The second principal component was positivelycorrelated with the abundance ofEg. ignitaand Eg.chalybeata, and negatively correlated with El. bom-biformis and El. chocoana. Stepwise discriminantanalysis for the habitat sites showed that four beespecies contributed to habitat differentiation (El.bombiformis, F3, 11 5.22, P 0.0410; El. cho-

coana, F3, 11

9.75, P

0.0056; El. cingulataF3, 11 6.08, P 0.0361; and Eg. flammea F3, 11 14.56, P 0.0022). The discriminant functionbased on the four bees as predictor variables col-lectively resulted in a perfect (100%) classificationof sites among habitats.

The difference between farm and forested siteswas consistent for both study years (Fig. 2a, b). Inthe first year PCA, the first principal componentexplained 32 percent of the variability and showeda differentiation between the farm and forestedsites. The second principal component explained

22 percent of the variability. This componentshowed a differentiation between secondary forestand old forest sites (Fig. 2a). In the second year,


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FIGURE 3. Temporal variation in euglossine bee cap-tures.

the first principal component explained 28 percentof the variability and showed a differentiation be-tween the farm and forested sites as in the first year.The second principal component explained 21 per-cent of the variability. This component also showed

a differentiation between three secondary forestsites and the other secondary forest site plus oldforest sites (Fig. 2b).

MORPHOMETRIC RANKS. Sorted on morphometricranks, bee captures were uneven both across and

within habitats. The proportion of large bees (H 6.27, df 2, P 0.04) and medium-sized,short-tongued bees (H 8.0, df 2, P 0.02)differed significantly among habitats. Large beesand medium, long-tongued bees overall were more

frequently captured at the farm (F2, 9

22.59, P 0.0003 and F2, 9 4.05, P 0.0441, respec-tively), while the abundance of medium, short-tongued bees did not vary among habitats (F2, 9 1.15, P 0.3592). On the farm, most of the cap-tured bees were large (57.1% of the bees, repre-sented by 6 spp.) and long-tongued (93.1% of thebees, represented by 14 spp.). Medium-sized, short-tongued bees were uncommon (6.9% of the bees).In both the secondary and the old logged forests,large bees were less abundant (19 and 17.6% ofthe bees, respectively), as medium-sized, short-

tongued bees were more frequent (39.0 and 40.3%of the bees, respectively). In contrast, there were nosignificant differences in the proportion of medi-um-sized, long-tongued bees among habitats (H1.50, df 2, P 0.47).

TEMPORAL VARIATION IN BEE ABUNDANCE. There was temporal variation in the abundance of eu-glossine bees over the two study years (F4, 36 5.76, P 0.0010; Fig. 3). This variation was par-tially due to abundance peaks associated with high

capture rates for some species. There was a generalincrease in the number of captured bees in the lastsix months of the study. More bees were capturedduring the last six months compared to the previ-ous period (F1, 5 13.3, P 0.015). Nevertheless,the effect of time on the number of species wasonly marginally significant (F6, 54 2.12, P 0.0654).

For two of the five most frequently collectedspecies, there were significant differences in thenumber of bees captured among sampling dates.Eulaema cingulata (Univar GG Epsilon 0.13;

F3, 25 9.57, P 0.0003) and Eg. ignita(UnivarGG Epsilon 0.14; F3, 26 4.40, P 0.0137)showed significant temporal variation. Large (Uni-

var GG Epsilon 0.16; F3, 30 7.84, P 0.0004) and medium-sized, long-tongued bees(Univar GG Epsilon 0.17; F3, 32 2.78, P0.0481) varied temporally, while small, short-tongued bees (Univar GG Epsilon 0.08; F2, 14 2.02, P 0.1729) did not.

DISCUSSION

Our analyses showed that the three habitats weredistinctly different in bee composition, with greaterdifferences between farm and forest habitats thanbetween the two forest habitats. Overall, our studyconfirmed, at a larger temporal scale, previous re-sults from a two-month study at the same sites(Sandino in press): male euglossine bees were morefrequently captured at farm sites than in either for-ested site. Capture abundances for some specieschanged seasonally and site samples changed fromone year to another, but the pattern of more abun-dant, richer, distinct captures at the farm sites pre-

vailed. We emphasize that we collected data froma single human intervention gradient, and so ourresults may not be applicable to other localities.


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Our results were consistent with two other re-cent studies of euglossine bee abundance. First, afour-month study had sampled 13 euglossine speciesfrom a logged and silviculturally treated plots inCosta Rica (Rincon et al. 1999). They found that

in the logged plots, the original old-growth forestwas lightly logged at irregular intervals during 19601989, while in the silviculturally treated plots, com-mercial logs were harvested at 10 m3/ha in 1989and 1990. The more disturbed silviculturally treatedplots had more euglossine bees visiting flowers thanthe logged plots. Second, a study had been con-ducted in Brazilian Atlantic Forest with a fragment-ed landscape (Tonhasca et al. 2002). When we per-formed a PCA analysis on their euglossine bee data,the species composition of that study revealed pat-

terns similar to those found in our study. The firstprincipal component differentiated fragmented fromcontiguous forest and the second principal compo-nent differentiated secondary from more preservedforest (disturbed but adjacent to the main forest). Astudy in the Brazilian Amazon, however, showed theopposite effect; there were fewer bees (species andindividuals) in experimentally deforested areas thanin the adjacent forest (Morato 1994). That studycompared pristine forest with a pasture on the bor-der of the forest, and the captures in the pasturemay have reflected the fact that bees live in the forest

and are able to forage in pasture. The differencesbetween those studies may have been due to differ-ences in the level of intervention among the studiedsites, since the Amazonian forest (Morato 1994) wasmore heavily disturbed than both the Brazilian At-lantic Forest and the logged forest in Costa Rica.

Based on the assumption that male euglossinecapture rates reflect actual abundance at the sampledhabitats, we propose that there is a morphometrictrend with large-sized, long-tongued bees and me-dium-sized, long-tongued bees foraging more at the

farm sites and medium-sized, short-tongued beesforaging more at secondary and mature forest sites.We hypothesize that the morphometric trend is cor-related with two factors: the effect of food resourceson proboscis length and the effect of microclimateon body size. On one hand, a long proboscis allowsaccess to nectar from an ample range of flowers,including the long tubular flowers of Costaceae, He-liconicaeae, Marantaceae, and Apocynaceae, which

were abundant in the disturbed farm habitat. Thelow frequency of short-tongued bees on the farmmay indicate that this habitat is very competitive

and that species are excluded because they do nothave access to nectar from deep-corolla flowers. Ad-ditionally, large size permits bees to tolerate high

temperatures and low humidity (May & Casey1983) that occur in the canopy (Roubik 1993; cf.Otero & Sallenave in press), which are expected inhighly disturbed habitats like the farm with its lowcanopy coverage and wide cleared patches. Large

species and some medium-sized (but long-tongued)species could thus be considered opportunistic, asthey seem better adapted to compete for the floralresources abundant in these disturbed habitats.Nonetheless, it should be noted that our samplingincluded only four of the seven hours that euglossinebees are active; thus, captures may have been biasedtoward large bees that forage earlier in the day (D.Roubik, pers. comm.). On the other hand, short-tongued bees may be more efficient at extractingnectar from shallow flowers than long tongued-bees.

Also, results from one other study seem to contradictours. In Brazil, larger Eulaema species were foundto be less tolerant of open spaces than Euglossaspe-cies (Peruquetti et al. 1999); thus, physiological traitsrelated to tolerance of disturbance may also influ-ence the most common species at each habitat. Dataon vegetation structure gave us no further insightinto habitat characteristics that contributed to maleeuglossine capture patterns, but as implied above,floral composition deserves more detailed study.

Our results for El. chocoanaare intriguing. Thisrecently discovered species (Ospina & Sandino

1997), despite being very abundant in a disturbedhabitat, appears to have a very limited distribution,apparently being endemic to the south of the Chocobiogeographic region (Sandino 1995b). The also re-cently described El. sororia (Dressler & Ospina1997), however, is abundant south of the Chocoregion (Sandino 1995a) and has been collected overa broader area, but was rarely collected in Anchicaya(Table 1). Why does El. chocoana, a bee species sofrequently captured in disturbed environments, havesuch a restricted distribution? In what kind of nat-

ural habitats did the species occur before humandisturbance patches were created in the region?Overall, our results show that some widely dis-

tributed (and the endemic El. chocoana), large bod-ied and/or long-tongued opportunistic species seemto occur more frequently in diversified farmlandsand disturbed forests within a mosaic that includesold logged forest. Could this mean that previouslyample foraging routes of male euglossine have de-creased in farmlands, as some have suggested (Jan-zen 1974, Aldrich & Hamrick 1998), or that op-portunistic species simply flourish at disturbed but

resource-rich habitats? Our results could be inter-preted in both ways. Similar multisite samplingschemes that simultaneously compare forests with


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adjacent monocultivars or non-diversified farm-lands are needed to fully understand the effects ofhuman land use on forest pollination dynamics.

ACKNOWLEDGMENTS

We thank P. Chacon and P. Silverstone-Sopkins for theirmentoring, support, and tolerance. Rodulfo Ospina, G.Nates, and R. Dressler provided taxonomical advice andfacilities. Roman Ospina made the unpublished results ofthe botanical survey in the area available. Jim Ackerman,P. Bayman, A. Sabat, N. Flanagan, D. Roubik, R. J. Mar-

quis, and anonymous reviewers commented on early ver-sions of the manuscript. T. A. Crowl and P. Thrall providedstatistical advice. This study was possible due to the datacollection and preliminary analyses made by M. Santaella,D. Daz, C. Restrepo, H. Asencio, A. Useche, M. I. Vallejo,O. Castro, C. Rentera, and I. Restrepo. Miller, William,

Tocayo, and F. Angulo gave us their expert field guidanceand assistance. We especially thank M. Angulo and thefamily of P. Angulo for their kindness and support. Permits

were provided by AFEPAL and the community of Guai-mia. This research was partially funded by a research grantgiven by the Fondo FEN-Colombia to the first author and

was supported under special arrangements and contracts bythe Fundacion Herencia Verde.

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