BIOTROPICA 35(4): 520–529 2003

Capture Rates of Male Euglossine Bees across a Human

Intervention Gradient, Chocó Region, Colombia1
J. Tupac Otero 2,3
Departamento de Biologı́a, Universidad del Valle, A.A. 25360, Cali, Colombia
and
Juan Carlos Sandino 4
Fundación Herencia Verde, A.A. 38302, Cali, Colombia

ABSTRACT
Euglossine bees are important pollinators of lowland Neotropical forests. Compared to disturbed habitats, undisturbed
ones have been previously characterized by higher abundance and diversity of euglossine bees. Most past studies have
relied 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 mosaic
of 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 secondary
forest (25.1%, 27 spp.), and 347 in the old logged forest (17.2%, 21 spp.). Eighty-one percent of the bees captured
belonged 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 secondary
forest. In contrast, Eg. hansoni, the sole short-tongued species among the five, was equally abundant in the two forest
habitats but occurred rarely on the farm. Additionally, habitats differed in bee composition. The high capture rates
for long-proboscis species at the farm may have been due to their ability to extract nectar from flowers with long
floral 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 hábitats
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 quı́micos para machos en sitios únicos por hábitat.
En este estudio realizamos muestreos basados en sitios múltiples en tres hábitats adyacentes (finca, bosque secundario,
y bosque maduro) a lo largo de dos años. Encontramos una mayor abundancia y diversidad de machos euglosinos en
los hábitats con mayor perturbación humana que en el bosque maduro. Después de 22 muestreos mensuales captu-
ramos un total de 2008 abejas representando 31 especies en cinco géneros: 1156 en la finca (57.6%, 21 spp), 505
en el bosque secundario (25.1%, 27 spp), y 347 en el bosque maduro (17.2%, 21 spp). El 80.8 por ciento de las
abejas capturadas pertenecı́an a las cinco especies más abundantes: Eulaema cingulata, El. chocoana, Euglossa hansoni,
Eg. ignita, y Eg. imperialis. Para estas especies encontramos diferencias en la frecuencia de captura entre hábitats.
Eulaema cingulata, El. chocoana, y Eg. ignita fueron más frecuentes en la finca, mientras que Eg. hansoni, la única de
las cinco con lengua corta, lo fue en los dos hábitats boscosos y Eg. imperialis en el bosque secundario. Adicionalmente,
los hábitats difirieron en composición de abejas. Lo resultados pueden deberse a que en la finca habı́a una mayor
oferta de néctar con acceso restringido que en los busques adyacentes. El néctar, por estar en flores de corolas profundas,
solo podı́a ser accedido por abejas de lenguas largas lo cual favorecı́a una mayor abundancia de euglosinas grandes
con lenguas largas en la finca que en los bosques adyacentes.

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

EUGLOSSINE BEES (EUGLOSSINI, APIDAE) ARE AMONG
the most important long-distance pollinators of
1 Received 18 November 2002; revision accepted 27 Au-
gust 2003.
2 Corresponding author; e-mail: tupac.otero@csiro.au
3 Current address: CSIRO Plant Industry, Australian Na-
tional Herbarium, GPO Box 1600, Canberra, ACT
2601, Australia.
4 Current address: Facultad de Biologı́a Marina, Universidad
Jorge Tadeo Lozano, Carrera 22-61, Bogotá, Colombia.
lowland Neotropical forests (Bawa 1990). The ca
200 species of this group (Kimsey & Dressler
1986) pollinate a vast array of plants at all succes-
sional stages (Gilbert 1980, Dressler 1982a, Acker-
man 1985). The taxonomy, ecology, and natural
history of euglossine bees are well documented
(Zucchi et al. 1969, Ackerman et al. 1982, Dressler
1982a, Janzen et al. 1982, Williams 1982, Roubik
& Ackerman 1987, Roubik 1989, Bonilla & Nates
1992, Armbruster 1993, Fernández 1995). Their
most remarkable feature is the fragrance-foraging

520

activity of males at flowers of several different plant
families and non-floral sources such as rotting logs
(Williams 1982, Whitten et al. 1993). The role of
euglossine bees as long-distance pollinators is crit-
ical because many plant species require cross-pol-
lination (Bawa 1990, Kress & Beach 1992, Oyama
1993) but exist at very low population densities
(Faber-Langendoen & Gentry 1991, Clark 1992).
Some authors have hypothesized that patches of
abundant resources resulting from deforestation
and farming practices may disrupt the foraging dy-
namics of euglossine bees in adjacent forests, and
thus the gene flow they mediate as pollinators may
be 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 given
localities (Janzen et al. 1982, Ackerman 1983,
Pearson & Dressler 1985, Powell & Powell 1987,
Roubik & Ackerman 1987, Sandino 1995a). Most
such samplings have been done at single locations
within habitats and at single habitats within land-
scapes. Capture rates are assumed to reflect actual
bee abundance at each habitat (Roubik 2001). Be-
cause foraging for nectar and fragrances and sexual
displays may each be performed at different and
distant sites (Janzen et al. 1982), we can assume
that capture rates reflect the use that males make
of each habitat. Some evidence supports this as-
sumption. Male euglossine bees may be collected
in higher frequency near the sites from which they
obtain food or fragrances (Ackerman 1983, Arm-
bruster 1993). Because they do not collect fra-
grances everyday, but do feed frequently, it seems
logical to suppose nectar distribution as a main, but
not 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 bait–capture samples from a single habitat
(Ackerman 1983, Armbruster 1993; cf. Roubik
2001), 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 deforestation
and fragmentation on euglossine bee communities
have been incomplete (Cane 2001) and based on
single-site sampling (Powell & Powell 1987, Becker
et al. 1991). The main objective of our study was
to document the differences in euglossine bee com-
munity structure through a human intervention
Euglossines across an Intervention Gradient 521
gradient at a lowland site in the Chocó biogeo-
graphic region of Colombia. To accomplish this
goal, we employed a repeated-measures design in
which, over a two-year period, we followed specific
sampling plots in three habitat types reflecting dif-
ferent levels of human disturbance. Specifically, we
asked: (1) Are euglossine bees more abundant and
diverse in forested habitats than in a farm?; (2) Do
capture rates differ among sites within habitats?; (3)
Do forested and farm sites differ in euglossine bee
composition?; (4) What bee characteristics may be
related 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 Guaimı́a
(38469N, 768579W) on the Anchicayá River. The
area, part of the biogeographical region of Chocó,
receives more than 7000 mm of annual rainfall and
has an average relative humidity of 96 percent.
Study sites were between 50 and 80 m elevation,
ranging from the riverbanks to low hills. The forest
is classified in the Holdridge system as transitional
between 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 Afro–American communities that fol-
lowed similar farming practices. The present hu-
man community and landscape have resulted from
the merging of traditional self-sufficient commu-
nities of farmers and miners with more recent col-
onizers. The present Afro–Colombian community
depends mainly on a subsistence economy based
on timber extraction, mining, agriculture, fishing,
and hunting. Farmlands are present all along the
Anchicayá River, and secondary forests abut the
farms and roads.
Based on their accessibility, we chose three dif-
ferent habitats that represented the most common
habitat gradients within the landscape (Tables 1
and 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 the
community organization AFEPAL, was a multi-
crop farm having several cultivars that included
both food and timber products (Table 1). It was
80 ha on the west margin of the Anchicayá River
and adjacent to secondary forests. The secondary
522 Otero and Sandino

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

Site Plant species

Farm
Secondary forest
Old logged forest
Cultivars: Chontaduro (Bactris sp.), green plantain (Musa paradisiaca), cassava (Mani-
hot esculenta), breadfruit (Artocarpus altilis), sugarcane (Saccharum officinale), and
borojó (Borojoa patinoi)
Dominant trees: Cedrela odorata (Meliaceae) and Cecropia spp. (Cecropiaceae)
Herbs reported as euglossine resources: Calathea spp., Heliconia spp., and Anthurium
spp.
Dominant trees: Mabea sp. (Euphorbiaceae), Cespedesia spatulata (Ochnaceae), Otoba
latialata (Myristicaeae), Miconia spp. (Melastomataceae), Wetinia quinara (Areca-
ceae), Chrysophillum sp. (Sapotaceae), Brosium utile (Moraceae)
Herbs reported as euglossine resources: Anthurium spp.
Dominant trees: Dussia lehemani (Fabaceae), Socratea exorrhiza (Arecaceae), Licania
duriflora (Chrysobalanaceae), Cecropia sp. (Cecropiaceae), Brosium utile (Moraceae),
and Symphonia globulifera (Clusiaceae)
Herbs reported as euglossine resources: Anthurium sp. and other plant species

forest had constant human intervention for timber
extraction and hunting by local people. The old
logged forest had intense commercial timber ex-
traction from the 1940s until ca 15 years before
our study, although selective timber extraction
along the Yesqueros stream was still frequent for
local uses. The old logged forest, however, was con-
tinuous with a natural undisturbed forest that is
part of the Buenaventura municipal reserve of San
Cipriano. In each habitat, we established four sam-
pling sites (Fa 1–4, SFo 5–8, and OFo 9–12) lo-
cated at least 200 m away from each other, in
agreement with Armbruster’s (1993) heterogeneous
results between sites.
HABITAT STRUCTURE. At each of four sampling
sites per habitat, we estimated the canopy height
using a clinometer, the average diameter of trees at
breast height (DBH), and the tree density as the
number of trees larger than 10 cm DBH within a
40 3 40 m plot. During the last months of our
study, a floristic profile was determined by other
researchers 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, we
placed three homemade, nonlethal traps (Sandino
in press) made from plastic dispensable bottles and
nylon stockings attached to the top in which the
bees arrived looking for the fragrance and were
added to a vial. The bees were able to enter the
trap to collect the fragrance, but once inside were
trapped in the stockings when attempting to leave
(Sandino 1995a). We used three different chemical
baits, one per trap at each site: 1-8 cineole, methyl
salycilate, and skatole. Bees were active between
0730 and 1430 h (Sandino, pers. obs.). Traps were
opened 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 using
a guide based on a previous reference collection
from the same locality and also by consulting spec-
imens available from other studies in the Chocó
region (Sandino 1995b) and elsewhere in Colom-
bia (Bonilla & Nates 1992). If a bee could not be
identified in the field, it was collected. Voucher
specimens were deposited in the bee laboratory at
the Universidad Nacional, Bogotá, 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,

TABLE 2. Structural measurements of the study sites (means 6 SD).

Trees .10 cm
Canopy height DBH/ha Average DBH
Site m (6SD) no. (6SD) cm (6SD)
Farm 12.4 (66.2) 5875 (63025) 50.1 (656.7)
Secondary forest 13.2 (64.4) 19,925 (64225) 27.3 (621.1)
Old logged forest 20.7 (66.5) 7625 (61625) 44.4 (639.2)

bees were marked on a wing using an indelible ink
marker (Outliner, Sakuraq, Hayward, California)
with a color specific to each habitat and then set
free. 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 euglossine
species (thus the name for the taxon), in some cases
exceeding body length. Species with short-folded
probosces are generally those Euglossa in which the
proboscis does not reach the abdomen. Euglossa
bees are more like honeybees in size, while Eufriesea
and 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 2–10 percent (Roubik 1992) within
species, we used the folded proboscis length and
the anterior wing length of bees to classify each
species in one of three morphometric classes: large
bees, with wings larger than 1.2 cm and folded
proboscis longer than 0.8 cm; medium-sized, long-
tongued bees, with wings shorter than 1.2 cm and
folded 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 Kruskal–Wallis test
(KW) on the canopy height and the tree density
data. 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 Anderson–Darling test. We calculated the
abundance, richness, the Shannon–Wiener diver-
sity index (H9), and the evenness (J9) according to
Zar (1999), and the Simpson’s index of dominance
(li) that measures the probability of randomly se-
lecting two individuals of the same species in a
community (Brower et al. 1997).
To test if species richness and abundance of
bees were equal across all habitats, we performed
repeated measures ANOVA (Zar 1999) on the nat-
ural log transformed data for number of bees and
the number of bee species. We repeated these anal-
yses using abundance data from the five most
abundant species, because those corresponded to
80.8 percent of the captures. Using the repeated
measures ANOVA design, we tested for differences
among sites within habitats (subject effects), differ-
ences among habitat types (treatment effects), and
Euglossines across an Intervention Gradient 523
the interaction between habitat type and time. Be-
cause we sampled over two years, our time effect
(22 mo) represented seasonal effects and temporal
dynamics. To determine whether or not the bee
community changed from the first to the second
year, two principal components analyses (PCA)
were conducted using a capture frequency matrix
of 31 species 3 12 sites including the bees captured
during both the first and second year of the study.
To determine whether or not there was an overall
differentiation in bee composition among habitats,
we performed a combined PCA with a matrix in-
cluding the samples from both years. To compare
the 12 communities for year 1 versus year 2, a PCA
was done with a matrix that included samples from
each year (June 1995–June 1996 vs. July 1996–
July 1997). All PCAs were performed using the
procedure PRINCOMP (SAS 1989). Finally, to
test differences among habitats, we used a stepwise
discriminant analysis using the 13 most abundant
species (PROC DISCIM; SAS 1989). Significant
variables (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 tree
density (Kruskal–Wallis, H 5 8.00, df 5 2, P 5
0.018) and in the average DBH (H 5 25.12, df
5 2, P , 0.0001) but not in canopy height (H 5
3.58, df 5 2, P 5 0.167). At the farm, the canopy
averaged 12.4 m (6SD 6.2) and tree density was
23.5 (6SD 12.1) per 1600 m2. The secondary for-
est was the most homogeneous of the habitats in
terms of the DBH classes and canopy height (13.2
m 6SD 4.4) and had the highest tree density (79.7
6SD 16.9 trees/1600 m2). The old logged forest
had the tallest canopy, 20.7 m (6SD 6.5), but rel-
atively low tree density (30.5 6SD 6.5 trees/1600
m2).
BEE ABUNDANCE AND DIVERSITY. Over the 22 sam-
pling dates, we collected 2008 male euglossine bees
belonging 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 in
the old logged forest sites, 347 males (17.2%) of
21 species. The number of captured bees was sig-
nificantly different across habitats (F2, 9 5 33.02,
P , 0.0001). More bees were captured on the farm
524 Otero and Sandino

TABLE 3. Total captures of male euglossine bees in each of the three study habitats. Fa: farm; SFo: secondary forest; and
OFo: old logged forest. The three morphometric ranks are L/L: large bees (with wings larger than 1.2 cm and
proboscis longer than 0.8 cm); M/L: medium-sized with long proboscis (with wings shorter than 1.2 cm and
proboscis 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: Simpson’s index of dominance. H9: Shannon–Wiener index. J9: evenness
index.

Morphometric
Species rank Fa SFo OFo Total
Eulaema aff. bombiformis L/L 24 20 2 46
El. chocoana L/L 294 27 3 324
El. cingulata L/L 329 38 50 417
El. sororia L/L 7 5 2 14
Euglossa allosticta M/L 27 6 6 39
Eg. asarophora M/L 1 8 9
Eg. bursigera M/L 2 9 2 13
Eg. chalybeata M/L 2 8 10
Eg. championi M/S 12 16 18 46
Eg. deceptrix M/S 4 1 5
Eg. dressleri M/S 3 1 7 11
Eg. flammea M/L 63 4 10 77
Eg. gorgonensis M/L 7 4 11
Eg. hansoni M/S 33 164 103 300
Eg. ignita M/L 276 76 85 437
Eg. imperialis M/L 17 107 21 145
Eg. aff. laevecincta M/L 1 1
Eg. mixta M/S 1 1
Eg. townsendi M/S 2 10 9 21
Eg. tridentata M/S 8 2 10
Euglossa sp. 9 M/S 14 2 16
Glossurela sp. 1 M/L 17 1 2 20
Glossurela sp. 9 M/L 14 5 19
sp. T 21 M/L 1 1
sp. T 23 M/L 1 1
sp. Q 24 M/L 1 1
Exaerete frontalis L/L 1 1
Ex. smaragdina L/L 3 3 6
Eufriesea pulchra L/L 2 1 1 4
Eufriesea sp. L/L 1 1
Aglae caerulea L/L 1 1
Total
Bees 1156 505 347 2008
Species 21 27 21 21
li 0.21 0.18 0.18 0.15
H9 0.84 0.92 0.93 0.97
J9 0.63 0.64 0.70 0.66

than in both the secondary forest and the old
logged 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 5 53.96, P , 0.0001), El.
chocoana (F2, 9 5 10.56, P , 0.0043), and Eg.
ignita (F2, 63 5 5.56, P 5 0.0267). The other two
species, Euglossa hansoni (F2, 9 5 1.69, P 5 0.2379)
and Eg. imperialis (F2, 9 5 3.30, P , 0.0842),
showed nonsignificant differences across habitats.
These five species accounted for 80.8 percent of
the captured males, none of which were more
abundant in the old logged forest than in other
habitats. Eulaema chocoana, El. cingulata, and Eg.
ignita were significantly more frequent at the farm
than at the other sites (X2 5 148.49, X2 5 82.32,
and X2 5 14.02, respectively; all tests df 5 2, P ,
0.005), while Eg. hansoni and Eg. imperialis were
captured most frequently in the secondary forest
(X2 5 266.70 and X2 5 109.07, respectively; both
with df 5 2, P , 0.005). The number of species
captured per habitat varied significantly (F2, 9 5
13.78, P , 0.0018). There was no significant dif-
 Euglossines across an Intervention Gradient 525

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.

ference in the H9 index (Kruskal–Wallis, H 5 1.38,

df 5 2, P 5 0.50) and evenness values J9 (H 5
2.28, df 5 2, P 5 0.31) for the different habitats
(Table 1).

BEE COMPOSITION. The first principal component

of the overall PCA based on both years explained
26 percent of the variability and separated farm
and forested sites (Fig. 2c). This component was
positively correlated with the abundance of El. cho-
coana, El. cingulata, and Eg. flammea and negatively
correlated with Eg. hansoni. The second principal
component explained 20 percent of the variability
and separated secondary forest sites from old forest
sites (Fig. 2c). Additionally, it separated one of the
farm sites (2) from the other three sites (1, 3, and
4). The second principal component was positively
correlated with the abundance of Eg. ignita and Eg.
chalybeata, and negatively correlated with El. bom-
biformis and El. chocoana. Stepwise discriminant
analysis for the habitat sites showed that four bee
species contributed to habitat differentiation (El.
bombiformis, F3, 11 5 5.22, P 5 0.0410; El. cho-
coana, F3, 11 5 9.75, P 5 0.0056; El. cingulata
F3, 11 5 6.08, P 5 0.0361; and Eg. flammea F3, 11
5 14.56, P 5 0.0022). The discriminant function
based on the four bees as predictor variables col-
lectively resulted in a perfect (100%) classification
of sites among habitats.
The difference between farm and forested sites
was consistent for both study years (Fig. 2a, b). In FIGURE 2. Plot of the two principal components of
the first year PCA, the first principal component the PCA based on the proportion of bees captured at the
explained 32 percent of the variability and showed 12 sites during the (a) first year, (b) second year, and (c)
combined first and second years. Sites Fa-1–Fa-4 are on
a differentiation between the farm and forested the farm (Fa); Sf-5–Sf-8 in the secondary forest (SFo);
sites. The second principal component explained and Of-9–Of-12 in the old logged forest (OFo).
22 percent of the variability. This component
showed a differentiation between secondary forest
and old forest sites (Fig. 2a). In the second year,
526 Otero and Sandino

the first principal component explained 28 percent

of 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 forest
sites and the other secondary forest site plus old
forest sites (Fig. 2b).

MORPHOMETRIC RANKS. Sorted on morphometric

ranks, bee captures were uneven both across and
within habitats. The proportion of large bees (H
5 6.27, df 5 2, P 5 0.04) and medium-sized,
short-tongued bees (H 5 8.0, df 5 2, P 5 0.02)
differed significantly among habitats. Large bees
and medium, long-tongued bees overall were more
frequently captured at the farm (F2, 9 5 22.59, P
5 0.0003 and F2, 9 5 4.05, P 5 0.0441, respec-
tively), while the abundance of medium, short-
tongued bees did not vary among habitats (F2, 9 5
1.15, P 5 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 the
bees, 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, FIGURE 3. Temporal variation in euglossine bee cap-
large bees were less abundant (19 and 17.6% of tures.
the bees, respectively), as medium-sized, short-
tongued bees were more frequent (39.0 and 40.3%
of the bees, respectively). In contrast, there were no
significant differences in the proportion of medi- var G–G Epsilon 5 0.16; F3, 30 5 7.84, P 5
um-sized, long-tongued bees among habitats (H 5 0.0004) and medium-sized, long-tongued bees
1.50, df 5 2, P 5 0.47). (Univar G–G Epsilon 5 0.17; F3, 32 5 2.78, P ,
0.0481) varied temporally, while small, short-
TEMPORAL VARIATION IN BEE ABUNDANCE. There tongued bees (Univar G–G Epsilon 5 0.08; F2, 14
was temporal variation in the abundance of eu- 5 2.02, P 5 0.1729) did not.
glossine bees over the two study years (F4, 36 5
5.76, P 5 0.0010; Fig. 3). This variation was par- DISCUSSION
tially due to abundance peaks associated with high
capture rates for some species. There was a general Our analyses showed that the three habitats were
increase in the number of captured bees in the last distinctly different in bee composition, with greater
six months of the study. More bees were captured differences between farm and forest habitats than
during the last six months compared to the previ- between the two forest habitats. Overall, our study
ous period (F1, 5 5 13.3, P 5 0.015). Nevertheless, confirmed, at a larger temporal scale, previous re-
the effect of time on the number of species was sults from a two-month study at the same sites
only marginally significant (F6, 54 5 2.12, P 5 (Sandino in press): male euglossine bees were more
0.0654). frequently captured at farm sites than in either for-
For two of the five most frequently collected ested site. Capture abundances for some species
species, there were significant differences in the changed seasonally and site samples changed from
number of bees captured among sampling dates. one year to another, but the pattern of more abun-
Eulaema cingulata (Univar G–G Epsilon 5 0.13; dant, richer, distinct captures at the farm sites pre-
F3, 25 5 9.57, P 5 0.0003) and Eg. ignita (Univar vailed. We emphasize that we collected data from
G–G Epsilon 5 0.14; F3, 26 5 4.40, P 5 0.0137) a single human intervention gradient, and so our
showed significant temporal variation. Large (Uni- results may not be applicable to other localities.

Our results were consistent with two other re-
cent studies of euglossine bee abundance. First, a
four-month study had sampled 13 euglossine species
from a logged and silviculturally treated plots in
Costa Rica (Rincón et al. 1999). They found that
in the logged plots, the original old-growth forest
was lightly logged at irregular intervals during 1960–
1989, while in the silviculturally treated plots, com-
mercial logs were harvested at 10 m3/ha in 1989
and 1990. The more disturbed silviculturally treated
plots had more euglossine bees visiting flowers than
the 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 first
principal component differentiated fragmented from
contiguous forest and the second principal compo-
nent differentiated secondary from more preserved
forest (disturbed but adjacent to the main forest). A
study in the Brazilian Amazon, however, showed the
opposite effect; there were fewer bees (species and
individuals) in experimentally deforested areas than
in the adjacent forest (Morato 1994). That study
compared pristine forest with a pasture on the bor-
der of the forest, and the captures in the pasture
may have reflected the fact that bees live in the forest
and are able to forage in pasture. The differences
between those studies may have been due to differ-
ences in the level of intervention among the studied
sites, since the Amazonian forest (Morato 1994) was
more heavily disturbed than both the Brazilian At-
lantic Forest and the logged forest in Costa Rica.
Based on the assumption that male euglossine
capture rates reflect actual abundance at the sampled
habitats, we propose that there is a morphometric
trend with large-sized, long-tongued bees and me-
dium-sized, long-tongued bees foraging more at the
farm sites and medium-sized, short-tongued bees
foraging more at secondary and mature forest sites.
We hypothesize that the morphometric trend is cor-
related with two factors: the effect of food resources
on proboscis length and the effect of microclimate
on body size. On one hand, a long proboscis allows
access 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. The
low frequency of short-tongued bees on the farm
may indicate that this habitat is very competitive
and that species are excluded because they do not
have access to nectar from deep-corolla flowers. Ad-
ditionally, large size permits bees to tolerate high
Euglossines across an Intervention Gradient 527
temperatures and low humidity (May & Casey
1983) that occur in the canopy (Roubik 1993; cf.
Otero & Sallenave in press), which are expected in
highly disturbed habitats like the farm with its low
canopy coverage and wide cleared patches. Large
species and some medium-sized (but long-tongued)
species could thus be considered opportunistic, as
they seem better adapted to compete for the floral
resources abundant in these disturbed habitats.
Nonetheless, it should be noted that our sampling
included only four of the seven hours that euglossine
bees are active; thus, captures may have been biased
toward large bees that forage earlier in the day (D.
Roubik, pers. comm.). On the other hand, short-
tongued bees may be more efficient at extracting
nectar from shallow flowers than long tongued-bees.
Also, results from one other study seem to contradict
ours. In Brazil, larger Eulaema species were found
to be less tolerant of open spaces than Euglossa spe-
cies (Peruquetti et al. 1999); thus, physiological traits
related to tolerance of disturbance may also influ-
ence the most common species at each habitat. Data
on vegetation structure gave us no further insight
into habitat characteristics that contributed to male
euglossine capture patterns, but as implied above,
floral composition deserves more detailed study.
Our results for El. chocoana are intriguing. This
recently discovered species (Ospina & Sandino
1997), despite being very abundant in a disturbed
habitat, appears to have a very limited distribution,
apparently being endemic to the south of the Chocó
biogeographic region (Sandino 1995b). The also re-
cently described El. sororia (Dressler & Ospina
1997), however, is abundant south of the Chocó
region (Sandino 1995a) and has been collected over
a broader area, but was rarely collected in Anchicayá
(Table 1). Why does El. chocoana, a bee species so
frequently captured in disturbed environments, have
such a restricted distribution? In what kind of nat-
ural habitats did the species occur before human
disturbance 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 seem
to occur more frequently in diversified farmlands
and disturbed forests within a mosaic that includes
old logged forest. Could this mean that previously
ample 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 sampling
schemes that simultaneously compare forests with
528 Otero and Sandino

adjacent monocultivars or non-diversified farm-
lands are needed to fully understand the effects of
human land use on forest pollination dynamics.
ACKNOWLEDGMENTS
We thank P. Chacon and P. Silverstone-Sopkins for their
mentoring, support, and tolerance. Rodulfo Ospina, G.
Nates, and R. Dressler provided taxonomical advice and
facilities. Roman Ospina made the unpublished results of
the 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 provided
statistical advice. This study was possible due to the data
collection and preliminary analyses made by M. Santaella,
D. Dı́az, C. Restrepo, H. Asencio, A. Useche, M. I. Vallejo,
O. Castro, C. Renterı́a, and I. Restrepo. Miller, William,
Tocayo, and F. Angulo gave us their expert field guidance
and assistance. We especially thank M. Angulo and the
family 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 grant
given by the Fondo FEN-Colombia to the first author and
was supported under special arrangements and contracts by
the Fundación Herencia Verde.

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