Diversity and Seasonality of Male Euglossine Bees (Hymenoptera: Apidae) in Central Panamá

Author(s): James D. Ackerman

Source: Ecology, Vol. 64, No. 2 (Apr., 1983), pp. 274-283
Published by: Ecological Society of America
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Ecology, 64(2), 1983, pp. 274-283
? 1983 by the Ecological Society of America

DIVERSITY AND SEASONALITY OF MALE EUGLOSSINE

BEES (HYMENOPTERA: APIDAE) IN CENTRAL PANAMA'

JAMES D. ACKERMAN
Department of Biology, University of Puerto Rico, Rio Piedras, Puerto Rico 00931

Abstract. Seasonal changes in species richness, composition, and abundance of male euglossine
bees were determined by weekly censusing of individuals attracted to 16 chemical baits. Bee popu-
lations were monitored for > 1 yr in the lowland tropical moist forest of seasonally dry Barro Colorado
Island (BCI), Panama. Male euglossine bees were also censused once every 4 wk at three nearby
mainland sites, two at low elevation, and one at a middle-elevation locality.
Among the lowland sites the male euglossine bee communities varied little; species composition,
dominance ranks, species' phenological profiles, and seasonal changes in bee abundance were similar.
Male bee populations at these sites were probably influenced by factors of similar timing and mag-
nitude. In contrast, the male bee community of the upland locality differed from lowlands in species
composition and timing of seasonal fluctuations in bee abundance.
At all census sites the male euglossine bee community had four genera (Eulaema, Euglossa,
Eufriesia, and Exaerete), 33-44 censused species, and low evenness of species abundance. On BCI,
the relative abundance of individuals in the four genera was not constant throughout the year. Species
richness and bee abundance were correlated; both fluctuated seasonally, and peaked in the early wet
season. However, species composition, evenness, and dominance ranks were virtually nonseasonal,
so some structural continuity existed in the male euglossine bee community.
Key words: bees; community structure; diversity; euglossine bees; Hymenoptera; neotropics;
phenology; pollination; population structure.

INTRODUCTION viewed by Zucchi et al. 1969, C. H. Dodson, personal

The abundance of most tropical insect species
changes seasonally (e.g., Janzen 1973, Wolda 1977,
1978b, Denlinger 1980, Wolda and Fisk 1981). Many
fluctuate as much as temperate and subarctic species
(Wolda 1978a, 1980), but some are virtually nonsea-
sonal (Ehrlich and Gilbert 1973, Wolda 1980). Popu-
lations of neotropical insect pollinators are no excep-
tion. For example, the flower-visiting wasps and bees
of seasonally dry Costa Rican habitats exhibited a
spectrum of seasonal abundance patterns (Heithaus
1979). These same complexities may appear in one
group of neotropical bees: the Euglossini (Hymenop-
tera: Apidae).
Euglossine bees are important pollinators of many
low- to middle-elevation plants (Dodson 1966, Zucchi
et al. 1969, Williams and Dodson 1972, Janzen 1974,
Ackerman, in press). These solitary, communal,
quasisocial bees (Michener 1974) are considered long
lived, but documentation is scant (Dodson 1962, 1966,
Janzen 1981a). They are wary, rapid fliers believed to
forage primarily at plants which produce few flowers
each day and bloom over a long period (Janzen 1971,
Williams and Dodson 1972, but see Ackerman, in
press). Food plants with this flowering strategy may
provide their pollinators with a more constant re-
source, and thus dampen fluctuations in abundance.
Nevertheless, populations of some species are be-
lieved to show considerable seasonal variability (re-
1 Manuscript received 9 October 1981; revised 2 April 1982;
accepted 7 April 1982.
communication).
Herein I present observations on both seasonally
variable and constant attributes of male euglossine bees
in central Panama. I examine changes in species rich-
ness, composition, and abundance of these bees.
MATERIALS AND METHODS
Baits
Male euglossines pollinate and collect floral fra-
grances from at least 650 species of orchids (R. L.
Dresser, personal communication) and a lesser num-
ber of species of other families. The fragrances col-
lected are ostensibly utilized as pheromones (Dod-
son 1975, Williams 1982). Many orchid floral
fragrances have been analyzed, and their compounds
identified (Hills et al. 1968, 1972, Dodson et al. 1969,
or Dodson 1970). The component chemicals have been
used to attract the otherwise elusive male bees (e.g.,
Adams 1968, Ricklefs et al. 1969, Dodson et al. 1969,
Williams and Dodson 1972, Kroodsma 1975, Janzen
198lb).
I monitored male euglossine bee populations by cen-
susing bees attracted to 16 chemical baits: cineole,
benzyl acetate, eugenol, vanillin, methyl benzoate,
methyl salicylate, methyl cinnamate, linalool, gera-
niol, skatole, f3-ionone, 2-phenyl ethyl acetate, 2-phe-
nyl ethanol, /3-myrcene, d-carvone, and benzyl ben-
zoate. All are naturally occurring compounds, and most
are known constituents of floral fragrances (Givaudan
Index 1961, Hills et al. 1968, 1972, Dodson 1970). Each
chemical was applied to separate 7 x 7 cm pads of

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April 1983 SEASONALITY OF MALE EUGLOSSINI
clean herbarium blotter paper. Most of the baits were
pipetted directly to the pads, but others required spe-
cial techniques. Vanillin crystals were mixed with ab-
solute ethanol to a supersaturated solution, which was
later applied to a pad. Skatole and methyl cinnamate
crystals were sprinkled on pads and gently melted over
a low flame. Most pads were kept saturated, and need-
ed rejuvenation during a census day to maintain at-
tractivity; replenishing frequency depended upon
evaporation rates. Unlike other baits, /3-ionone pads
were not maximally attractive when saturated, and re-
quired only a few drops each day.
Census technique
From 0830 to 1230 I presented the chemical baits.
This 4-h time block lies within the peak fragrance col-
lecting activity period of male euglossine bees (=0700-
1300 in central Panama [J. D. Ackerman, personal ob-
servation ]). At 15-min intervals I recorded all visitors
to each of the compounds. A bee was a visitor if the
species was observed to land on the bait, brush the
pad, and then transfer the compounds to the hind tib-
iae in the manner described by Evoy and Jones (1971).
Only vouchers and taxonomically difficult species were
captured. Determinations of these were verified by R.
L. Dressler. Most individuals collected compounds
relatively undisturbed and for as long as they desired.
All species attracted to baits were counted. The first
individual of a species to arrive at a given chemical
was included in the 15-min census following arrival.
Each week I presented the chemicals over two or three
consecutive days because it was not possible to effec-
tively monitor all 16 chemicals at once.
The presence of bees was not obviously related to
incident radiation (Inouye 1975, Janzen et al. 1982),
but during rainstorms most bees left the baits to seek
shelter. Census days were usually repeated when rain
fell between 0830 and 1230 for >30 min. Nevertheless,
data retained and taken on census days with periods
of rainfall were not significantly different from rainless
day data of the following or previous week at three
highly attractive chemicals (Wilcoxon matched-pairs
signed-ranks two-tailed test [Daniel 1978]; cineole:
preceding week, N = 10, T = 16, P > .1, following
week, N = 10, T = 20, P > . 1; methyl salicylate: pre-
ceding week, N = 7, 7 = 12, P = .11, following week,
N 7, TI' 10,P > . 1;skatole: preceding week, N =9,
71 22, P > .1, following week, N = 9, T = 10, P >
. 1).
Studv sites and census periods
Male euglossine bee populations were monitored at
four localities. The primary study site was on Barro
Colorado Island (BCI), in Lake Gatun, Panama. Every
week from mid-February 1979 to mid-March 1980, I
baited for bees at the Tower Clearing. Thereafter, I
baited once every 4 wk through June 1980.
The Tower Clearing lies at the summit and approx-
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275
imate geographical center of BCI, at 164 m elevation.
The site lies at the eastern edge of a plateau and at a
transition between old and young forest (R. B. Foster,
personal comr/unication). The vegetation of BCI is
classified as semievergreen tropical forest (Knight 1975,
system of Beard 1944) or tropical moist forest (Tosi
1971, system of Holdridge et al. 1971). Barro Colorado
Island has a tropical monsoon climate (Koppen cli-
matic classification), and annual rainfall ranges from
190 to 360 cm (Croat 1978). The climate is distinctly
seasonal with a dry period of 3-4 mo beginning near
mid-December. The dry season offers the most hours
of sunshine and the strongest winds. I have divided
BCI's climate into four 13-wk seasons: dry, early wet,
mid wet, and late wet. This time frame is used in the
data analysis and discussion. The actual dry season
extends -2 wk earlier and later than delimited here.
The late wet and early wet seasons represent climat-
ically transitional periods. A more detailed description
of the climate, history, geology, and vegetation is in
Croat (1978).
I monitored male euglossine bee populations at two
lowland sites in Parque Nacional Soberania, which is
in the same vegetation zone as BCI. These were cho-
sen to test the applicability of the BCI censuses to
similar, nearby areas. One was northeast and across
Lake Gatun from BCI, 400 m west of the tracks of the
Ferrocarril de Panama on Frijoles Road along a ridge
at 80 m elevation. The forest in the area was young,
mostly <100 yr old. Male bees were censused at all
16 chemical baits once every 4 wk from February 1979
to March 1980.
The other lowland site was on a ridge, 100 m el-
evation, and 10 km northeast of Gamboa along Pipe-
line Road. The vegetation in the area is similar to that
of BCI but perhaps more diverse (A. H. Gentry, per-
sonal communicationo. I baited once every 4 wk from
October 1979 through June 1980. Schedule constraints
permitted only I d of baiting, so only eight of the more
powerful attractants were used: cineole, benzyl ace-
tate, eugenol, vanillin, methyl benzoate, methyl salic-
ylate, methyl cinnamate, and skatole. Otherwise the
censusing technique was the same as employed at the
other sites.
The third mainland census site was at ~840 m, in
the premontane wet forest (Holdridge Life Zone Sys-
tem, Tosi 1971) of Cerro Campana, southwest of Ca-
pira, Panama Province. Here the climate is cooler and
wetter, and the dry season is tempered by cloud drip.
Floristically and structurally the forest is quite differ-
ent from BCI; e.g., epiphyte loads are heavy, and the
canopy is low. The populations of male euglossine bees
were monitored with all 16 chemical baits every 4 wk
from February 1979 to March 1980.
The more frequent and protracted baiting program
on BCI permits a more detailed analysis of seasonal
patterns in male euglossine bee populations. Unless
otherwise stated, all statistical analyses pertaining only
276 JAMES D. ACKERMAN Ecology, Vol. 64, No. 2

to BCI censuses employ data of 52 consecutive weeks

beginning mid-March (week 11) 1979. The less fre- 30 a
Cn _
quent monitoring at the secondary sites will be for
general comparisons among sites. For the statistical 026_ ~~0. se
analysis of these, I used only BCI data of the week o * *- ..
immediately preceding the secondary site census. In en
comparing Pipeline Road and BCI censuses, I ana- U,
0
22 0 00@ 0*
LLI " **
lyzed only the data of the eight chemical baits em-
0.
ployed at both sites. U_
_
Sampling assumptions Z 8
0~~~~~~~~
0
14_
00
Uniformity of the sample area was measured indi- 2
z
rectly by examining the possible functional relation-
ship between wind velocity and abundance of bees 10 l l l l l l l l l l l l l l
attracted to baits. The rainless 0830-1230 censuses at 10 18 26 34 42 50 6
cineole and vanillin (relatively high and low volatility WEEK OF THE YEAR
compounds, respectively) from the Tower Clearing DRY EARLY MID WET LATE DRY
were compared with hourly wind run data for 0800- WET WET
1200 collected at the Laboratory Clearing (1.4 km dis- FIG. 1. Weekly species richness of male euglossine bees
tant) by the Smithsonian Tropical Research Institute at baits on Barro ColoradoIsland.
Environmental Sciences Program. Wind conditions
prevailing at the island summit corresponded with those
at the Laboratory.
Male euglossine bee activity at artificial baits may nearby, Kennedy 1978, R. L. Dresser, personal coin-
not reflect activity at natural sources. To test this, I Inunication), El. leucopyga, Eg. cyanura, Ef purpur-
monitored fragrance collecting activity every 2 wk for ata (J. D. Ackerman, personal observation), Ex. den-
I yr (beginning March 1979) at inflorescences of a con- tata, and Ex. trochanterica (Kimsey 1979). Of these,
tinuously blooming population of Spathiphyllum fried- only Eg. cyanura was frequently encountered on BCI
richsthalii (Araceae) in Fuertes Cove, BCI. This species foraging at fragrance and food flowers.
is visited by many euglossine bees. From 0900 to 1300 Weekly species richness of the four genera com-
I recorded the number of individuals of each species bined fluctuated from 12 to 30 species, with the great-
collecting floral fragrances and compared the data with est range occurring in the late wet season (Fig. 1). A
the preceding and then the following week's censuses majority of Euglossa, Eulaelna, and Exaerete species
of the same species to baits at the Tower Clearing, I were recorded in every season. Eufriesia were more
km distant. seasonal, and only one of nine species was observed
Emergence patterns of adult bees may invoke shifts in at baits every season (Table 1). The other genera av-
local population levels. Because nests are difficult to eraged 28-34 census weeks per species, but Eufriesia
find, I sought indirect evidence of emergence events by species averaged only 12 wk apiece.
monitoring the age structure of the male bee commu- On BCI, 21 842 bees were recorded during the study
nity. I examined bees attracted to Tower Clearing baits year. The abundance of bees was strongly seasonal,
for wing wear from November 1979 until June 1980. I and the greatest number was attracted to baits from
designated an "old" bee as one with at least two nicks the middle of the dry season through the early wet
in its forewings. If the bee censuses were largely un- (Fig. 2, Table 1). The abundance of bees observed
biased samples of male euglossine populations in the during the 16-wk overlap period of 1980 was consistent
area, and if abundance changes were due to emergence with censuses of the previous year.
patterns, then significant fluctuations in abundance of Weekly total bee abundance and species richness
bees should correspond to age structure shifts. for the 1-yr period were highly correlated (Spearman's
rank correlation coefficient [Daniel 1978], r, = .79, P <
.0001). The weekly median number of individuals per
RESULTS
species was also correlated with species richness (r=
Barro Colorado Island .58, P < .0001).
The Tower Clearing baits attracted 44 species of All four genera exhibited seasonal fluctuations in
male euglossine bees (Table 1) distributed among four abundance. Nevertheless, Euglossa, the most abun-
genera: ELfriesiia (Ef), Euglossa (Eg.), Eulaelcna (El.), dant genus, maintained its dominance throughout the
and Exacerete (Ex.). The latter is a nest parasite of year. Eulaena was the next most numerous, followed
other large euglossines (Kimsey 1979). Only six species by Eufriesia and Exaerete (Table 1). The relative
known or expected to occur on BCI were not attracted abundance of individuals among genera was not pro-
to any of the 16 chemical baits: El. seabrai (reported portionately constant throughout the seasons (G-test

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April 1983 SEASONALITY OF MALE EUGLOSSINI 277

TABLE 1. Seasonal abundance of male euglossine bees at 16 chemical baits on Barro Colorado Island, Panama, from week
II 1979 to week 10 1980. (Week I begins on I January.) See Fig. 4 for visual representation of abundance profiles. Data
for each season represent the total number of bees recorded in censuses in the 13-wk period.

Season
Abundance No. weeks Dry Early wet Mid wet Late wet
Species profile recorded (Wk 2-14) (Wk 15-27) (Wk 28-40) (Wk 41-1) Total
Euglossa
alllosti(ta V 49 134 151 31 40 356
azureov iridlis V 36 27 85 30 10 152
bursigera VI 50 83 173 57 94 407
chalmpioni IV 21 9 16 9 34
cognalta V 29 55 107 6 2 170
crassipunctata V 49 47 88 15 32 182
cy anaspis III 20 13 2 3 8 26
cxvbelil IV 12 1 15 2 2 20
despecta V 50 226 302 51 42 621
dissitmla V 47 624 728 38 70 1460
dodsolii III 18 12 5 3 12 32
dress/lri VI 32 15 26 9 23 73
flainineia 4 4 4
gorgonlelisis IV* 3 2 1 3
hansoni VI 40 101 268 14 23 406
heinic(llora 9 12 2 14
heterosticta V 44 57 127 15 31 230
ignite I I I
ignii'entris IV 17 13 11 1 25
imperialis V 52 1405 1961 910 892 5168
inixta VI 45 109 191 33 30 363
purpura II 6 12 5 17
saJpphirinal III 43 32 62 32 25 151
towt'nsendi 1 2 2
tridentata V 52 1971 3264 296 138 5669
turbinif(x 2 2 2
variabilis V 40 254 207 12 14 487
illosil'clntris 5 1 7 8
Totals 5203 7822 1557 1501 16 083
Eufrle(sial
afnilso(chlora II* 1 4 4
('rOnI'alC V 22 5 1 130 41 177
corus(a II 9 220 220
Iuc(kei II* 2 4 4
luciwitra IV 17 4 28 4 36
ornlata I 17 2 211 30 243
pulchral I 24 28 57 4 89
SsclIniidtiana II 11 1 80 81
surinalnientsiys I 9 32 32
Totals 37 349 429 71 886
Eu/lael ia
bombfi/ornis IV 14 15 9 24
cilngulata V 52 507 795 233 153 1688
Inerialia V 52 392 518 133 172 1215
nigrit(I V 52 691 731 158 206 1786
pol/ichrotnal 3 3 3
Totals 1608 2044 524 540 4716
Exacreut
troontalis III 47 31 43 40 23 137
snlarag'dina IV 13 8 10 1 1 20
Totals 39 53 41 24 157
Grand totals 6887 10 368 2551 2136 21 842
No. species 33 41 28 30 44
- Ascertained from Frijoles Road and Pipeline Road censuses.

of independence [Sokal and Rohif 1969], G = 1071, 9 Eufriesia were most numerous in the early and mid
df, P < .005). Euglossa and Eulaena were abundant wet seasons, but the species were erratically abundant
in the dry season and peaked in the early wet, before (e.g., Ef. (orusca and Ef. concava). Exaerete was more
plunging to low levels in the mid and late wet seasons. abundant in the early and mid wet seasons, but its wet-

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278 JAMES D. ACKERMAN Ecology, Vol. 64, No. 2

2,000 for association, using Kendall's coefficient of con-

en
(/)0 cordance (Daniel 1978). The ranks are highly associ-
< 1,000 .
.0 0 0
ated (W = .671, 43 df, P < .005), and indicate that the
o A,... * 0 0
species dominance rank order is generally maintained
- 600 * 0.0.
throughout the year. However, the probability of ob-
[ 400 0 taining a particular rank order is dependent on sample
m 0~~~~~~~~~~~~~~~ size and evenness (Jumars 1980). The latter is not a
< 200 - problem here because the pattern of distribution of
individuals among the species is similar for all seasons
0o (Fig. 3). The analysis of very abundant species with
X 100
rare ones may, however, bias the concordance test. I
m
60 compared rank orders of abundant species (1000+ in-
z
dividuals observed in censuses in I yr) separately from
40
5 15 25 35 45 3 13 23 the common ones (100-999 individuals), and I elimi-
WEEK OF THE YEAR nated the rare species (< 100 recorded individuals). The
DRY EARLY MID LATE DRY EARLY dominance rank orders of the abundant species were
WET WET WET WET maintained through the seasons (W = .629, 5 df, .006 >
FIG. 2. Weekly abundance of individual male euglossine P > .004). However, no significant correlation of rank
bees attracted to chemical baits on BCI, during 1979-1980. orders existed for the common ones (W = .353, 14 df,
P > .1). Among this group were three Eufriesia spp.,
which were conspicuous for their abrupt seasonal ap-
season decline was gradual, not dramatically abrupt pearance and departure at baits. Without the Eufrie-
as in the other genera (Table 1). sia, the rank orders of common species were main-
The curve of relative abundances of species is steep tained seasonally (W = .522, 1I df, .025 > P > .01).
(Fig. 3). This indicates low evenness and, conversely, The overviews of male euglossine bee phenologies
high dominance by a few species. The two most abun- give no indication how the component species con-
dant species in any season accounted for 45-50% of tribute to the general seasonal pattern. The shapes of
the individuals observed. These species were usually species abundance curves were diverse, and may be
Eag. imnperialis and Eg. tridentata. The relative abun- roughly categorized into six basic types: cornucopia,
dance curves are similar among seasons and have vir- big bang, steady state, modified steady state, single-
tually the same slope as the abundance curve for the peak steady state, and multiple-peak steady state (Fig.
year. The lack of seasonal differences in relative abun- 4, terminology modified from Gentry [1974]). The phe-
dance of bee species is underscored by examining the nological pattern for most species was determined by
number of species in three abundance classes for each inspection and is listed in Table 1.
season (1-10, 11-100, 100-1000+ bees). The propor-
tion of species in each class does not change signifi- Frijoles Road
cantly over the seasons (G = 6.01, 6 df, .5 > P > .1). Census data of Frijoles Road and other secondary
For each season I ranked the species according to sites in a form similar to Table I are in Ackerman
their abundances. The four rank orders were tested ( 1981). In 13 censuses spanning I yr (beginning March

100 DRY SEASON EARLYWET MIDWET LATE WET BCI, 52 CENSUSES

60
40
20

10 0
z

~0.6 01 203 02 04 02 m0 0 02 0 1 0 04
0.4 -

0.2 -

0 .1 -- m s g m _ _ _ _ _ _ _ _

10 20 30 0 1020 3040 010 20 0 102030 010 2030 40

SPECIES RANK
FIG. 3. Relative abundance curves of male euglossine bees on Barro Colorado Island. Points represent species plotted
by their abundance, as a percent of the total, against the species' rank in the sequence of species from most to least abundant.

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April 1983 SEASONALITY OF MALE EUGLOSSINI 279

Imx
C)
LU
U-

TIME (ONE YEAR)

FiG. 4. Schematic abundance profiles of euglossine bees. I: Cornucopia; II: Big bang; III: Steady state; IV: Modified
steady state; V: Single-peak steady state; VI: Multiple-peak steady state. See Table I for examples in each category.

1979), 41 species came to the 16 chemical baits. Species
composition at Frijoles Road was 96% similar (Soren-
sen's coefficient of similarity [C8], Southwood 1978)
to that observed on BCI. The seasonal abundance pat-
tern was similar to that observed on BCI, but the peak
activity period was relatively brief (Fig. 5). The com-
munity of male euglossine bees sampled at Frijoles
Road revealed the same pattern of species dominance
and relative lack of evenness as on BCI (Fig. 6). There
was also no difference in the overall dominance ranks
at the two sites (r, = .876, P = .001). As on BCI, Eg.
tridentate and Eg. imperialis accounted for >50% of
the individuals censused in I yr.
Pipeline Road
The first census at Pipeline Road was not until late
October 1979, so only nine censuses are available for
analysis. The eight chemicals attracted 35 species. In
the same period of time and in an equivalent number
of censuses, 38 species came to the same eight baits
on BCI. Species compositions of the two sites were
similar (C, = 90%). Bee abundance was usually great-
er than on BCI (Fig. 5). Nevertheless, the relative
species abundance curves of the two sites are very
similar (Fig. 6). A few species accounted for more than
half the individuals. The overall rank order of species
abundance of Pipeline Road was highly associated with
the species ranks of BCI (r, = .846, P = .001).
Cerro Camnpana
In I yr, 44 species of male euglossine bees arrived
at the 16 chemical attractants. For the equivalent num-
ber of censuses (13) only 38 species arrived at baits
on BCI. The similarity of the two sites was only 78%,
the lowest value of all paired site comparisons. The
number of bees attracted to baits on Cerro Campana

fn 2,000 - o0-BCI - o-BCI _--BCI

0--FRIJOLESRD. RD. *--CERRO CAMPANA
< *--PIPEINE D V...LESSEF. COANCAVA
m V~*FIJLSR.-IPLN
3 1,000

600

200 /

. . . . . . .I . . .
D 100 19918017 198 17 18

BCI SEASONS ~ ~ ~ 'I

5 15 25 35 45 3 13 45 3 313 5 15 25 35 45 3 13
1979 1980 1979 1980 1979 1980
WEEKS OF THE YEAR

DRY EARLY MID LATE DRY LATE DRY EARLY DRY EARLY MID LATE DRY
WET WET WET WET WET WET WET WET
BCI SEASONS

FIG. 5. Seasonal abundance of male euglossine bees at Frijoles Road, Pipeline Road, Cerro Campana, and Barro Colorado
Island. Where possible, BCI data represent the census average of the weeks before and after the secondary site census. The
vertical bar represents the range.

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280 JAMES D. ACKERMAN Ecology, Vol. 64, No. 2

100 B oBCI OBCI

60 APIPELINERD AFRIJOLESRD ACERROCAMPANA
40
0
20 L

10 0

GA
_ sib _AjA

0.6 a'_CD

0.1
_4 Ii9 , __ , I - ,
0 0 20 30 40 0 10 20 30 40 0 10 20 30 40 50
SPECIES RANK
FIG. 6. Relative abundance curves of Pipeline Road, Frijoles Road, and Cerro Campana compared with corresponding
censuses of Barro Colorado Island.

was highly seasonal like that observed at all the low-
land baiting sites; however, the peak activity period
was one season later, occurring in the early wet and
mid wet season (Fig. 5). There was resurgence of the
total number of bees to baits in the late wet season,
but this was entirely due to a tremendous influx of Ef.
conccVa (Fig. 5). The relative abundance of individual
species censused on Cerro Campana shows that, once
again, a few species accounted for most of the indi-
viduals, although four instead of two species account-
ed for 50% of the bees censused. Nevertheless, the
resultant relative abundance curve differs little from
that of BC! censuses (Fig. 6). The dominance ranks
of the two sites are markedly different, and there is
no association between the two species ranks (r8=
.314, P = .83). The dominants were Eg. miaculilabris,
Eg. deceptrix, El. cingulata and Ef. conca Va. The two
Euglossa species were not found on BC1 or at either
secondary lowland site. I recorded the lowland dom-
inants, Egs. imperialis and Eg. tridentata, in nearly
every census on Cerro Campana, but they ranked 14
and 10, respectively, in overall abundance.
chemicals was probably attained regardless of wind
conditions.
Eleven species of male euglossine bees commonly
collected fragrances from both Spathiphyllum fried-
richsthalii inflorescences and the Tower Clearing baits;
these were El. cingulata, El. meriana, Ex. frontalis,
Ef. lucifera, Ef. pulchra, Eg. mixta, Eg. crassipune-
tata, Eg. cognata, Eg. villosiventris, Eg. purpurea,
and Eg. sapphirina. The number of male bees visiting
the aroid per inflorescence is correlated with the over-
all abundance pattern of the same I I species to chem-
ical baits (with preceding Tower Clearing census: r, =
.791, P < .002; with following census: r, = .551, P =
.004, Fig. 7). The censuses probably reflect fragrance-
collecting activity at natural sources.
The age structure of male bee populations changed
ZZ 250-
0.30 3z
2200 -

Sampling assumptions
C l_
X)
H 0
X0
~~
~~~~~~~~~~0
~(n Z
- 150 - O ?- 0.20
om< 0
For each of the four seasons there was no correla- 0 0
HLJ

tion between the 4-h wind run average of each census 0D

U)<
100 1 2 35 4j
day and the number of bees arriving to cineole or van- 0
(O) sources (16 chemiclsprsentedat >C0.10 i
illin (Cineole: dry season, r, = -.067, P = .84; early M ~~~~~~0
00 - 0-
-< 50 - a *.*0 o Z LLJ
wet, rs = .20, P = .65; mid wet, r. = .297, P = .33; Z
Fn0 0~~~
**.cjo
U)
U)
QL

late wet, r, =.678, P= .097. Vanillin: dry season, 0)F 04 OL

r, = -.055, P = .87; early wet, r8= -.15, P = .67; :D

~~~~
atnatra 0
5
LO
15
ptihlu
25
U rercshli
~~~~~~~~~~0
35 45 3
n
13
rifiia:D
i

mid wet, r, = .146, P = .68; late wet, r, = .524, P = 1979 WEEK OF THE YEAR 1980
16). Thus, the abundance of bees to baits appears
FiG. 7. Fragrance foraging activity of male euglossine bees
independent of wind conditions at least over the 4-h at natural (0; Spathiphyllumfriedrichsthalii)and artificial
census period. The maximum active space of the (0) sources (16 chemicals presented at the Tower Clearing).

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April 1983 SEASONALITY OF MALE EUGLOSSINI 281

50 1,000 habitats. Because euglossine bees are known to fly

long distances (e.g., Dressier 1968, Williams and Dod-
a son 1972), it is possible that the seasonal patterns of
I 40 800
male Euglossini in central Panama and BCI in partic-
9 ~ ular are primarily caused by movement patterns of
species. There is evidence that bees fly across Lake
Ui3?020
.0-Q~~~~~~~~~~~. 600 Gatun to BCI (Janzen 1971, D. W. Schemske, person-
al communication, Ackerman 1981, Ackerman et al.
-.%
~0 6 6 m 1982) and come from distant habitats. Orchid pol-
0 48206 5
M~~0 1 0 400
linarium loads of euglossine bees are easy to identify
'I I~~~~~~~~~~-J
O f . p. . w (Dressler 1968, 1976a, Ackerman 1981), and several
bees observed on BCI and Frijoles Road carried or-
a- chid pollinaria of genera not known to occur in the
C1 0 area. Two Eg. sapphirina had Sievekingia fimbriata
48 52 4 8 12 16 20 24
pollinaria, two Eg. Inixta carried Kefersteina cf. lac-
WEEK OF THE YEAR tea, one El. nigrita had a Cycnoches aureum pollinar-
FIG. 8. Changes in age structure and abundance of male ium, and two El. ineriana had Houlletia tigrina pollen
euglossine bees on Barro Colorado Island. The percent old loads. The bees may have emigrated from wetter for-
bees sampled of a given species was weighted according to
the relative abundance of that species in the censused pop- est of the Atlantic coast or higher elevations where
ulation. these orchids are known to occur (J. D. Ackerman,
personal observation, R. L. Dressler, personal coIn-
Inunication, Dressler 1976b).
as abundance of bees fluctuated. In the late wet season Seasonal patterns may not be induced by migration.
when bee abundance was lowest, the percentage of If migrants cause major increases in bee abundance,
old bees was high. As the number of bees increased, then foreign pollinarium loads should appear during
the relative abundance of old bees decreased. Later in immigration periods. This was not the case. Four of
the year, bee abundance leveled and then dropped as the seven carriers of foreign pollinaria were sighted
the percentage of old bees recorded increased (Fig. 8). during declining- or low-abundance periods of their
The censuses reflected probable emergence patterns, species. In addition, these carriers were rare. Only 7
and may thus be indicative of actual male bee abun- of 35 668 bees censused at the lowland sites bore pol-
dance. linaria of foreign orchids, which represents 0.4% of
the total pollinarium carriers observed.
DISCUSSION In some situations, male euglossine bees exhibit site
Populations of some euglossine bee species may re- fidelity (Dodson 1966, Kroodsma 1975, L. S. Kimsey,
main active but reduced in size and locally restricted personal communication, Ackerman 1981, Ackerman
during certain times of the year. During the mid and et al. 1982), and some bees may be reluctant to
late wet seasons, Exaerete s'naragdina and Eufriesia leave their habitat. Attempts to draw bees out of the
ltcijera ceased arriving at Tower Clearing baits. The forest and across pastures or open water using baits
former was consistently observed at the Laboratory yielded dramatically reduced species richness and
Clearing 1.4 km away and collected cineole there (J. abundance relative to the composition of the source
D. Ackerman, personal observation). The latter species areas (Ackerman 1981, Janzen et al. 1982). Perhaps
was often observed obtaining fragrances from Spathi- the most compelling argument against the migration
phylluanfriiedrichsthalii inflorescences in Fuertes Cove. hypothesis is that an increase in the proportion of young
The absence of at least some species at artificial bees corresponded with the abrupt increase in total
baits appears to reflect actual adult inactivity. Inde- bee numbers. Seasonal fluctuations in abundance are
pendent of present results most Eufriesia of Panama probably caused by local nesting and emergence pat-
(excluding EJ lucifera and Ef. pulchra) were thought terns of the bees. Thus, some individuals do indeed
to be highly seasonal (R. L. Dressler, personal corn- move about and fly long distances, but massive move-
lnunication), with males and females generally active ments of bees are not very likely responsible for most
simultaneously (L. S. Kimsey, personal co/nlnunica- of the observed seasonal phenomena.
tion). Flight activity was believed to be a wet-season There was little site variation in male euglossine
phenomenon, and emergence of adults to be often dra- populations of lowland central Panama. Species com-
matically synchronized (N. H. Williams, C. H. Dod- positions, dominance ranks, relative abundance curves,
son, and R. L. Dressler, personal coinInunication). overall bee abundance patterns, and species pheno-
The present data corroborate these observations. logical profiles were similar among BCI, Pipeline Road,
Janzen (198 la) hypothesizes that in seasonally se- and Frijoles Road sites. The differences were relative-
vere habitats male euglossine bees may be transient ly minor. At Frijoles Road there was a short peak
and seek a variety of resources in different and distant abundance period, and at Pipeline Road bees were

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282 JAMES D. ACKERMAN
generally more numerous (Fig. 5). Furthermore, some
species were more common at some sites than others.
For example, Eg. dressleri was more numerous on the
mainland than on the island (Table 1). Nevertheless,
the similarities among the lowland sites are striking
and suggest that these localities represent a single hab-
itat type for the male euglossine bee community.
Euglossine bee population and community charac-
teristics of dissimilar or geographically isolated habi-
tats are often distinct (review by Zucchi et al. 1969,
Ricklefs et al. 1969, Janzen et al. 1982). A comparison
of Cerro Campana and the isthmian lowland sites was
no exception. The species composition, rank order of
species dominance, and seasonal changes in bee abun-
dance on BCI were more dissimilar to that of Cerro
Campana than to either of the other lowland sites.
Even the phenological behavior of some species resi-
dent in both upland and lowland areas differed. In the
lowlands, Eg. inperialis had a single-peak steady-state
pattern (Fig. 4), whereas on Cerro Campana it exhib-
ited a steady-state profile. Given these differences be-
tween the geographically proximate Cerro Campana
and lowland sites, male euglossine bee communities
should be similar at sites only within a restricted geo-
graphical area and of similar topography, climate and
vegetation.
Wolda (I1977, 1978b, 1980) notes that abundances of
many tropical forest insect populations show consid-
erable annual variability, and that nearly all species
show little seasonal constancy in numbers. This study
was not sufficiently long to determine between-year
population constancy, but several facets of the male
euglossine community fluctuated seasonally. Species
richness and bee abundance were correlated, and in
the lowlands they peaked from the middle of the dry
season through the early wet. Also, seasonal re-
sponses of the species were diverse and are illustrated
by the array of phonological profiles (Fig. 4, Table 1).
Not all attributes of the male euglossine bee com-
munity were seasonally variable. A few species had
aseasonal abundance patterns, as is found in other
groups of tropical spiders and insects (Robinson et al.
1974, Wolda 1980). The rank orders of species abun-
dances did not shift significantly. That is, the same
species were generally dominant in all seasons. Fur-
thermore, the distribution of individuals among the
species was maintained at a low level of evenness.
Thus, the seasonal shifts had no appreciable effects
on other structural aspects of the community.
With a rise in species richness, evenness might in-
crease if critical local resources are seasonally con-
stant. But in lowland central Panama, resource levels
change. Most massively blooming and abundant nec-
tar hosts of euglossine bees are in flower during peak
bee activity. Later in the wet season when bee activity
wanes, most nectar host plants are scattered and gen-
erally produce few flowers per day (Ackerman, in
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All use subject to JSTOR Terms and Conditions
Ecology, Vol. 64, No. 2
press). These resource shifts may be responsible for
the seasonal changes in the euglossine bee community.
ACKNOWLEDGMENTS
I am indebted to Drs. N. H. Williams, R. L. Dressier, and
D. W. Roubik, and Ms. A. M. Montalvo for many fruitful
discussions and logistic and technical assistance. Discussions
with Dr. C. H. Dodson were helpful in formulating this proj-
ect. I thank all of the above and Drs. D. R. Strong and K.
P. Sebens for criticizing the manuscript. The Smithsonian
Tropical Research Institute and its staff provided logistic sup-
port. Drs. R. Silberglied, N. Smith, and D. Windsor were
particularly helpful. This project was financed by a Smith-
sonian Institute Predoctoral Fellowship to the author and a
Smithsonian Scholarly Studies Grant (#1234SO01) to D. W.
Roubik.
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