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Journal of Insect Science: Vol. 11 | Article 97 Franco and Gimenes
Journal of Insect Science | www.insectscience.org 1
Pollination of Cambessedesia wurdackii in Brazilian campo
rupestre vegetation, with special reference to crepuscular
bees
Emanuella Lopes Francoa* and Miriam Gimenesb
Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Avenida Transnordestina, S/N,
Bairro Novo Horizonte, 44036-900 Feira de Santana – BA, Brasil
Abstract
Cambessedesia wurdackii Martins (Myrtales: Melastomataceae) is presumably endemic to the
Chapada Diamantina, Bahia State, Brazil. A majority of the species of this family are pollinated
by diurnal bees that buzz the floral anthers to collect pollen. The present work examined the
interactions between C. wurdackii and visiting bees, focusing on temporal, morphological, and
behavioral features, especially in regards to the crepuscular bees Megalopta sodalis (Vachal)
(Hymenoptera: Halictidae) and Ptiloglossa aff. dubia Moure (Hymenoptera: Colletidae). The
study was undertaken in an area of campo rupestre montane savanna vegetation located in the
Chapada Diamantina Mountains of Bahia State, Brazil, between August/2007 and July/2008.
Flowering in C. wurdackii occurred from April through July, with a peak in May. A total of 592
visits by diurnal and crepuscular bees to the flowers of C. wurdackii were recorded, with a
majority of the visits made by M. sodalis and P. dubia (92%) near sunrise and sunset. The anthers
of C. wurdackii are arranged in two tiers, which favors cross pollination. The morphological,
temporal and behavioral characteristics of M. sodalis and P. dubia indicated that they were
potential pollinators of C. wurdackii, in spite of the fact that the colorful and showy flowers of
this species are more typical of a diurnal melittophilous pollination syndrome.
Keywords: montane savanna, Colletidae, Halictidae, Megalopta,Ptiloglossa
Correspondence: a* emanuella_bio@yahoo.com.br,bmiriam.gimenes@uol.com.br, *Corresponding author
Editor: Todd Shelly was editor of this paper.
Received: 9 March 2010, Accepted: 4 April 2011
Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits
unrestricted use, provided that the paper is properly attributed.
ISSN: 1536-2442 | Vol. 11, Number 97
Cite this paper as:
Franco EL, Gimenes M. 2011. Pollination of Cambessedesia wurdackii in Brazilian campo rupestre vegetation, with
special reference to crepuscular bees. Journal of Insect Science 11:97 available online: insectscience.org/11.97
Journal of Insect Science: Vol. 11 | Article 97 Franco and Gimenes
Journal of Insect Science | www.insectscience.org 2
Introduction
The botanical family Melastomataceae is well
represented in tropical and subtropical regions
of the Americas (Renner et al. 2001). It is the
sixth largest Angiosperm family in Brazil in
terms of the number of species, with
representatives being found in many diverse
habitats, such as the Atlantic Forest (Melo et
al. 1999), Amazonian Forest (Renner 1987),
Cerrado (savanna) (Renner 1990), dune and
beach-front areas (Alves-dos-Santos 1999),
and especially in areas of campo rupestre
(high-altitude open, rocky areas) (Romero and
Martins 2002). The genus Cambessedesia
occurs in Brazil and many species occur in
campo rupestre vegetation (Martins 1984),
while others are found in areas of cerrado
(Joly 1987). Cambessedesia wurdackii
Martins (Myrtales: Melastomataceae) is
geographically restricted to Bahia State in the
Chapada Diamantina Mountains (Martins
1984).
Characteristic of the family Melastomataceae,
species of Cambessedesia have flowers with
rich colors and poricidal anthers. These
flowers are classified as melittophilous and
are visited almost exclusively by bees that
buzz the anthers to release their pollen (Vogel
1978; Faegri and Van Der Pijl 1979; Renner
1989). In a study of pollination and the
reproductive systems of Cambessedesia
hilariana in areas of campo rupestre and
cerrado vegetation in São Paulo State, large,
diurnal bees of the genera Centris,Bombus,
and Xylocopa were the principal pollinators
(Fracasso and Sazima 2004).
Plants with floral morphologies similar to
those seen in the genus Cambessedesia are
melittophilous, and this syndrome is generally
associated with the diurnal foraging of certain
bees. Nonetheless, some bee species
belonging to four of the seven bee families
(Colletidae, Andrenidae, Halictidae and
Apidae) have independently adopted the habit
of foraging when there is very little daylight,
concentrating their activities during the late
evening hours or at daybreak (Hopkins et al.
2000; Wcislo et al. 2004; Warrant 2008). The
evolution of this activity pattern is probably
related to the exploitation of richer floral
resources and avoidance of competitors,
predators and parasites with diurnal habits
(Wicslo et al. 2004; Kelber et al. 2006).
In general, bee species that have crepuscular
habits, such as species of the genus
Ptiloglossa (Hymenoptera: Colletidae)
(Roberts 1971) and Megalopta (Halictidae)
(Janzen 1968; Kelber et al. 2006), forage just
before daybreak and just after sunset. In a
study on the relationship between the sizes of
the ocellus of some crepuscular bee species
and their foraging activity, it was noted that
ocellus size is not directly proportional to
head size, principally among crepuscular and
nocturnal species in which ocellus size tended
to be larger (Kerfoot 1967).
The knowledge of the floral resources utilized
by nocturnal and crepuscular bees is still
incipient and quite limited. Researchers that
have analyzed pollen samples from nests of
species within the genus Megalopta in tropical
regions have identified more than 40 plant
species with diurnal and/or nocturnal anthesis
belonging to the families Bombacaceae,
Anacardiaceae, Guttiferae, and
Melastomataceae (Roulston 1998; Wicslo et
al. 2004). Megalopta centralis visited the
flowers of Solanum spp. (Solanaceae) and
Calathea insignis Petersen (Marantaceae) in
Costa Rica (Janzen 1968). Megalopta spp.
were considered as pollinators of Parkia
Journal of Insect Science: Vol. 11 | Article 97 Franco and Gimenes
Journal of Insect Science | www.insectscience.org 3
velutina Benoist in the Amazon region
(Brazil) (Hopkins et al. 2000), and species of
the genus Ptiloglossa were recorded visiting
flowers of Solanaceae (Linsley and Cazier
1970), Melastomataceae (Roberts 1971), and
Ipomoea (Convolvulaceae) (Schlising 1970).
The purpose of this study was to describe
interactions between C. wurdackii and visiting
bees, focusing on the morphological,
behavioral and temporal aspects of the visits
of the bees in relation to temperature, relative
humidity, light intensity and daily light/dark
cycle; and especially in terms of the
crepuscular bee species Megalopta sodalis
Vachal (Hymenoptera: Halictidae) and
Ptiloglossa aff. dubia Moure (Colletidae).
Methods
Study area
The present study was undertaken in an area
of campo rupestre vegetation inside the
Mucugê Municipal Park (12º 59' 18.5" S x 41º
20' 27.8"W; at 950 m altitude), the
headquarters of the “Sempre Viva” Project.
This vegetation is characterized principally by
a herbaceous-shrub physiognomy with a high
degree of endemism. The region has
extensive areas of exposed rock and a low
water-retention capacity. The plant families
showing the greatest species richness in the
campos rupestre vegetation of the Chapada
Diamantina Mountain Range are Orchidaceae,
Poaceae, Asteraceae, Velloziaceae,
Bromeliaceae, and Melastomataceae (Harley
1995; Conceição et al. 2007a, 2007b). The
local climate is semi-humid, with irregular
annual rainfall between 600 and 1500 mm.
Average temperatures vary between 13º C in
the dry season (April to September) and 30º C
in the rainy season (October to March),
although large variation may occur between
years (Stradmann et al. 1998).
Environmental and meteorological data
Data on rainfall, relative humidity, and
monthly average temperature from August
2007 to July 2008 were obtained from the
meteorological station at the Municipal Park.
Sunrise and sunset times were obtained from
the Brazilian National Observatory
(http://euler.on.br/ephemeris/index.php).
Temperature, relative humidity, and light
intensity data were collected in the field
during the observations of floral visitors, with
at least one measurement being made every
hour. Light intensity was measured using a
digital luximeter (Lutron LX-107,
www.lutron.com) at a distance of 100 cm
from the soil.
Floral Biology
The individuals of C. wurdackii that were
studied were sparsely distributed woody
shrubs approximately 50 cm tall growing on
rocky and inclined river margins. To evaluate
the flowering phenology of C. wurdackii, 11
individual plants were marked and monitored
from August 2007 through July 2008.
Observations of floral biology and floral
visitors were performed on three days during
June 2007, late May - early June, and late
June - early July 2008 (months with great
numbers of flowers) (total observation period
of 9 days).
The timing of floral opening and the durations
of the flowers were followed in 10 flowers on
different plants. The stigmas were cut off and
submerged in 10% hydrogen peroxide
solution. Stigma receptivity was evaluated
based on the intensity of effervescence
(Zeisler 1933 in Dafni and Maués 1998) on
three pre-anthesis buds (at a time close to, but
still before the full opening of the flowers)
and on three flowers at different phases of
anthesis (3 hours, 27 hours, 59 hours, and 75
Journal of Insect Science: Vol. 11 | Article 97 Franco and Gimenes
Journal of Insect Science | www.insectscience.org 4
hours after opening). To determine the
presence of osmophors, ten flowers were
submerged in a solution of 1:10.000 neutral
red: tap water for 10 min. Flowers were then
rinsed with tap water (Vogel 1963 in Ormond
et al. 1981). To determine the presence of
pigments that absorb in the ultraviolet
spectrum, ten flowers were placed in a glass
container and exposed to ammonium
hydroxide vapor. (Scogin et al 1977).
Ten flowers from different plants were chosen
to measure the corolla diameter, anther length,
style length , the width of the upper anther
clusters, and the distance between the upper
anther cluster and the stigma.
Floral visitors
In order to observe the activities of the floral
visitors, a 100 m2 plot was selected in the
study area during each field trip in a locality
with large number of flowers. This plot was
used to make behavioral observations of the
bees and to record their visiting activities
during three days each month (04:30 - 19:30)
(before dawn to after sunset). The total
number of visits of each bee species was
noted during two intervals of 15 minutes
during each hour of observation. The bee visit
count was based on the number of times each
bee buzzed the flowers for pollen collection.
In addition to these regular observations, three
days of observations were made throughout
the night (18:00 - 06:00) in June 2007 in order
to determine if the flowers of C. wurdackii
were visited during these hours.
Observations of floral visitor behavior were
made during each hour interval in the field,
mainly at the moment when a bee arrived near
each flower. The way the insect’s body made
contact with the stigma and its behavior while
collecting the floral resource were noted.
Photographs and digital films were made of
the floral visits to aid in these analyses.
To analyze the morphological characteristics
of each bees species, 3-10 individuals were
collected to measure their body length
(between the median ocellus and the end of
the abdomen) and intertegular width (the
distance between wing bases). Additional
measurements were made of the width of the
median ocellus and the width of the head,
following Kerfoot (1967). The ratio of median
ocellus width to head width was related to the
light intensity at the time of each species’
peak of visitation.
The collected bees were deposited in the Prof.
Johann Becker Entomological Collection of
the Museu de Zoologia da UEFS, and
vouchers of C. wurdackii were deposited in
the Herbarium of the Universidade Estadual
de Feira de Santana (HUEFS).
Data analysis
The flowering pattern of this species was
classified using the scale developed by
Newstron et al. (1994) according to its
frequency and duration.
The frequency of bee visits to the flowers was
calculated based on the percentage of the total
number of visits to a species in relation to the
total number of visits observed.
Spearman’s correlation was used (at p < 0.05)
to analyze the influence of climatic factors on
flowering, as well as the influence of climatic
factors during the day on the numbers of bee
visits.
Results
Flowering in C. wurdackii occurred from
April to July, with a total of 150 flowers
Journal of Insect Science: Vol. 11 | Article 97 Franco and Gimenes
Journal of Insect Science | www.insectscience.org 5
observed in April, 1062 in May (flowering
peak), 185 in June, and only 1 in July. The
flowering phase coincided with diminishing
values of: the photophase (total period of
available light during the day), precipitation,
and the average temperature (Figure 1). Of the
variables analyzed, only flowering and the
average values of the photophase (rs = -0.75)
demonstrated a significant negative
correlation.
The flowers of C. wurdackii are of the open
type - pentamerous and zygomorphic - with
green sepals and oval petals with two showy
colors: yellow at the basal quarter and orange
colored above, reflecting iridescently in the
sunlight. Pollen is the only floral reward
offered to insect visitors. The corolla tube had
a diameter of 18 ± 0.92 mm. The style was
10.9 ± 0.57 mm long. The stamens were free
and didynamous, each being composed of a
filament and an elongated yellow anther that
terminated in an apical pore. The anthers were
arranged in two clusters: an inferior group
formed by three large anthers (mean ± SD =
4.4 ± 0.5 mm of length) that were grouped
together with the style and stigma and another
upper group formed by seven smaller anthers
(3.2 ± 0.55 mm of length), totaling 10 anthers.
The flowers had a sweet smell that was most
intense in the afternoon and evening. This
odor probably arises from osmophores located
on the corolla and on the tips of the anthers
(as indicated by treatment with neutral red).
Tests with ammonium hydroxide vapor did
not indicate the presence of pigments that
reflect ultraviolet light.
Pre-anthesis initiated about 24 hours before
the flowers began to open and was
characterized by the elongation of the style
and the exposition of the stigma beyond (and
therefore outside of) the floral bud. The petals
gradually began to open at approximately
01:00, while the anthers remain doubled over
in the bud with their pores facing the base of
the filaments. As the petals continued to open
(about 2 hours after initiating anthesis) the
anthers were presented in 2 clusters, giving
the flower a strongly zygomorphic symmetry.
The stigma was now located beyond the
anther pores, characterizing herkogamy.
Anthesis terminated at about 05:00 when the
petals were totally extended. Twenty-four
hours after floral opening the petals gradually
acquired a pallid aspect and finally abscised
after 72 to 80 hours. The stigma was receptive
for the entire period from pre-anthesis to petal
fall.
A total of 582 visits were recorded by bees
belonging to three families and seven species
(Table 1). The present study represents the
first report for Bahia State of P. dubia (67%
of the total number of visits) and M. sodalis
(25.3%), and these species were observed to
be the most frequent visitors to C. wurdackii.
The other species collectively made only 7.7%
of the total visits. P. dubia,M. sodalis and
Euglossa sp. visited C. wurdackii flowers
during all of the observation months (Table 1).
The greatest number of floral visits occurred
at the end of June and the beginning of July
2008 (92% of the total number of visits), 5%
of the visits occurred at the end of May and
beginning of June 2008, and 2% of the visits
occurred in June 2007.
Table 1. Bees visitors to flowers of Cambessedesia wurdackii in an
area of campo rupestre vegetation in Mucugê, Bahia State, Brazil.
N = number of visits; width (intertegular distance), and lengh
(distance between the median ocellus and the end of the abdomen)
of the bees.
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Journal of Insect Science | www.insectscience.org 6
In spite of the fact that all of the bee species
visiting C. wurdackii flowers buzzed their
anthers, no species was able to embrace both
the upper and lower clusters of anthers at the
same time. A bee would generally embrace
only the upper group of anthers (which served
as their landing platform), although these
insects would occasionally also buzz the
lower anther group. When a bee buzzed the
upper anthers, the entire flower would vibrate
and the pollen would be liberated from both
the upper and lower anthers. The pollen
liberated from the upper anthers was generally
deposited on the ventral portion of a bee’s
thorax and later transferred to the scopae or
corbiculae. The pollen from the lower anthers
was generally deposited on the posterior
portion of the abdomen of the largest bee
visitors where it could come in contact with
floral stigmas during subsequent floral visits,
and this pollen was apparently not actively
transferred to the scopae by those bees (Figure
2).
The average widths of C. fuscata,P. dubia,B.
atratus, and X. cearensis were approximately
the same size as the average width of the
group of upper anthers (mean ± SD = 5.0 ±
0.6 mm), while the remaining bee species
were thinner (Table 1). Despite differences in
width, the only species that was not able to
embrace all of the upper anthers during their
floral visits was P. cf. callaina. The distance
between the upper group of anthers and the
stigma (9.0 ± 1.35 mm) was slightly less than
the average length of the bees (Table 1).
However, the bees curved their abdomens
while visiting the flowers, thus diminishing
their overall effective length; the smallest bees
(P. cf. callaina and Euglossa sp.) therefore
did not touch the stigma during their visits.
M. sodalis generally fly slowly and then
amble over the inflorescences, touching the
stigma of the flower. This bee generally
remained for approximately 20 seconds on
each flower. They tended to spend more time
on the flower than the other species of bee
visitors. P.dubia, B. atratus, and X. cearensis
all made rapid visits, remaining for about 3
seconds on each flower.
M. sodalis and P. dubia had crepuscular and
bimodal activity patterns, with one activity
peak in the early morning and another in the
late evening (Figure 3). Floral visits by M.
sodalis and P. dubia began at 05:20 (about 40
minutes before sunrise). M. sodalis terminated
its visits at 05:35, and P. dubia at 06:40
(Figure 3).The greatest numbers of visits
during the early morning hours occurred
between 5:20 and 5:30 for M. sodalis, and for
P. dubia, the greatest numbers of visits
occurred between 5:30 and 5:40, with an
average temperature near 16.0º C. Both of
these bee species visited flowers of C.
wurdackii around sunset, but visits were less
frequently than at sunrise: at 17:40 - 18:00 for
M. sodalis (N = 9), and at 17:20 – 17:40 for P.
dubia. The greatest numbers of visits by P.
dubia during the late evening occurred at
17:30 (N = 67), with an average temperature
near 21.0º C. During the entire activity phase
of visits by M. sodalis the light intensity
varied from < 1 lux to 47 lux and by P. dubia
varied from < 1 lux to 2720 lux (Figure 3).
The Spearman correlation values relating the
numbers of visits of each of the bee species to
C. wurdackii flowers to the microclimatic data
(collected during each day) were significant
only for the visits of P. dubia and M. sodalis.
The correlation was positive for the relative
humidity and negative for temperature and
light intensity, with the greatest correlation
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Journal of Insect Science | www.insectscience.org 7
values being seen for the latter variables
(Table 2).
The analysis relating the sizes of the median
ocellus and the head demonstrated significant
differences between bee species with
crepuscular and diurnal habits (Figure 4). The
nocturnal and crepuscular species (M. sodalis
and P. dubia) had the highest ratios between
ocellus size and head width, thus having the
largest ocelli even though they did not have
the widest heads (Figure 4). The ratios
between ocellus size and head width when
compared with the light intensity values at the
time of peak visitation (Figure 5) indicated
that the bee species with proportionally larger
ocelli visited C. wurdackii flowers during
times of lower light intensity than did bee
species with proportionally smaller ocelli.
Discussion
The flowering of C. wurdackii in the area of
campo rupestre examined was of intermediate
duration with a single flowering peak in May
(according to the classification of Newstron et
al.1994). In a study of flowering of C.
hilariana in an area of rupiculous and cerrado
(savanna) vegetation at 880 m altitude in São
Paulo State (Brazil), Fracasso and Sazima
(2004) noted that the flowering pattern of C.
hilariana is long and annual, with flowering
from September to July and a peak from
October to December. According to this study
C. hilariana provides abundant resources for
bee species during a large part of the year, a
situation that was not observed with C.
wurdackii in the present study.
The flowering activity of C. wurdackii and the
general morphology of their flowers are
consistent with the majority of the
Cambessedesia species (Martins 1984). C.
wurdackii flowers, however, emit a sweet
aroma, while Martins (1984) noted that the
flowers of the genus Cambessedesia are
odorless. An acrid-saponaceous odor was also
reported for flowers of C. hilariana (Fracasso
and Sazima 2004).
Both the time of day when the flowers of C.
wurdackii first open and the placement of the
floral verticils during anthesis represent a
pattern quite different from that described for
C. hilariana (Fracasso and Sazima 2004). At
the initiation of anthesis in C. hilariana the
flowers demonstrated actinomorphic
symmetry, which only changed approximately
three hours later with the shifting of the
position of the anthers, style and stigma into a
single group in the lower part of the flower
(Fracasso and Sazima 2004). This pattern of
placement of the floral whorls occurs in much
the same manner in other species of
Melastomataceae (Melo and Machado 1996).
In C. wurdackii, however, the anthers form
two clusters (an upper and a lower) when
floral opening begins. This placement makes
it difficult for the visiting bees to embrace all
of the anthers at once, although it is
commonly observed in other plant species
having poricidal anthers buzzed by bees
(Melo and Machado 1996; Fracasso and
Sazima 2004; Oliveira-Rebouças and
Gimenes 2004). The floral anatomy of C.
wurdackii may favor cross-pollination as
pollen is liberated from the lower anther group
(indirectly, as a result of the buzzing of the
upper group) and becomes attached to the end
of the abdomen of most of the visitor bees
Table 2. Values of the Spearman correlation (p<0.05) relating
climatic variables measured during the day (temperature, relative
humidity, and light intensity) with the numbers of visits of Ptiloglossa
aff. dubia and Megalopta sodalis to flowers of Cambessedesia
wurdackii in an area of campo rupestre vegetation in Mucugê, Bahia
State, Brazil.
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where it is not easily transferred to the scopae
and corbiculae. Additionally, herkogamy
(which is a common characteristic in
Melastomataceae flowers [Renner 1989])
causes the stigma to touch the visiting bee’s
abdomen before the anthers are buzzed, thus
reducing the chances of self-pollination
(Fracasso and Sazima 2004).
The flowers of C. wurdackii remain open for
more than 24 hours and can be visited by
diurnal, crepuscular, and nocturnal animals. In
an investigation of pollination in Silene alba
(Caryophyllaceae), Young (2002) observed
that the flowers of this species remained open
for more than 12 hours and were visited by
animals with diurnal or nocturnal habits. The
flowers of C. wurdackii were visited by bees
with diurnal (C. fuscata,B. atratus,X.
cearensis,P. cf. callaina, and Euglossa sp.) as
well as crepuscular habits (M. sodalis and P.
dubia), with the latter bee species being more
frequent. The flowers of C. hilariana
remained open for approximately 60 hours in
the southern region of Brazil, but only
received visits from diurnal bees (the genera
Centris,Bombus, and Xylocopa),although this
result was certainly influenced by the fact that
their observations were limited to only the
diurnal period (Fracasso and Sazima 2004).
The activities of the crepuscular bees (M.
sodalis and P. dubia) in the present study
appear to be influenced by light intensity. The
numbers of visits of both bee species
diminished greatly as light intensity increased,
and a significant negative statistical
correlation was observed between the number
of visits and light intensity. The importance of
light intensity to the daily activity of
Megalopta genalis (a crepuscular bee) was
also observed by Kelber et al.(2006) in
Panama.
In addition to light intensity, temperature also
appears to exercise an important role in the
daily activity of crepuscular bee visitors to C.
wurdackii flowers, as there was a significant
negative statistical correlation between the
temperature and floral visits. P. dubia, the
largest and most pilose bee in the present
study, was observed visiting C. wurdackii
flowers more frequently than M. sodalis
during periods of lower temperatures. The air
temperature acts on the thermoregulation
mechanisms of bees and other insects, but can
be modified by their morphological
characteristics (including size, number of
bristles, and the color of their integument)
(Herrera 1995). Additionally, some studies
have established a relationship between
buzzing behavior and the capacity of these
bees to forage at low temperatures for the
vibration of their flight muscles during
buzzing helps increase their body temperature
(Buchmann 1983; Renner 1989).
Large ocelli have been viewed as an essential
morphological adaptation for bees foraging
under low light (Kelber et al. 2006; Warrant et
al. 2006; Warrant 2008; Somanathan et al.
2008). P. dubia and M. sodalis examined in
the present study have both ocelli and head
sizes typical of nocturnal and crepuscular bees
(Kerfoot 1967). Ocelli have been shown to be
the principal organs responsible for night
vision in the Hymenoptera, while compound
eyes are principally used during the day
(Warrant et al. 2006). The strong relationship
between the proportionally large size of their
median ocelli and the capacity of P. dubia and
M. sodalis to forage under conditions of low
light intensity was likewise observed by
studying other species of bees (Kerfoot 1967;
Kelber et al. 2006), ants (Moser et al. 2004),
and wasps (Warrant et al. 2006) with similar
crepuscular and nocturnal habits.
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In spite of the fact that all of the bee visitor
species employed the same behavior patterns
in removing pollen from the flowers of C.
wurdackii (buzzing the anthers), not all of
them could be considered potential pollinators.
The smaller species (P. cf. callaina and
Euglossa sp.) did not come into contact with
the stigma during their floral visits, while the
other diurnal species (C. fuscata,B. atratus,
and X. cearensis) were observed successfully
transferring pollen grains to the stigmas of
these flowers. Nonetheless, considering the
low numbers of visits of C. fuscata,B. atratus,
and X. cearensis , they can only be considered
occasional pollinators of C. wurdackii. On the
other hand, in light of their morphological
characteristics, the high frequency of their
visits, and their behavior in the flower the
crepuscular species, M. sodalis and P. dubia,
were considered potential pollinators of C.
wurdackii.
The floral anatomy of C. wurdackii indicates a
melittophilous syndrome (Faegri and Van Der
Pijl 1979). Although the yellow and orange
colors of the flowers of C. wurdackii are
considered to be typical attractants of diurnal
bees, C. fuscata,B. atratus, and X. cearensis
appeared to have only a small role in
pollination in the present study. The flowers
of C. wurdackii were visited more frequently
by crepuscular bees, and these insects were
also considered to be potential pollinators. In
studying the pollination of Parkia velutina
Benoist (Leguminosae: Mimosoideae) by
nocturnal bees of the genus Megalopta,
Hopkins et al. (2000) proposed that nocturnal
melittophily in the genus Parkia represented
an intermediate stage in the evolution of
chiropterophily to entomophily within this
genus, with the presence of characteristics of
both syndromes (although the flowers also
emitted a strong sweet odor that would
preferentially attract insects). The flowers of
C. wurdackii also produce a sweet odor that
becomes stronger towards the end of the day.
This characteristic is not common among the
Melastomataceae and may represent an
important attractant for the crepuscular bee
species that pollinate these flowers.
The present study of pollination in C.
wurdackii demonstrated that although these
flowers have characteristics normally
associated with the attraction of diurnal
visitors, crepuscular visitors were actually
potential pollinators. A number of workers
have reported that plants that maintain their
flowers open for more than 12 hours receive
visits from nocturnal, crepuscular, and diurnal
pollinators (Slauson 2000; Young 2002).
Accordingly, studies of floral visitors to plants
with flowers that remain open for long periods
of time must necessarily include observations
made during their entire receptive period.
Acknowledgements
The authors would like to thank Leandro M.
Santos for identifying Megalopta sodalis; Dr.
Favízia F. de Oliveira (UFBA) for identifying
the other bee species; Msc. Andrea K.A.
Santos (UEFS) for identifying Cambessedesia
wurdackii; the administration of the Mucugê
Municipal Park for their permission to work in
the area; UEFS for financial support; and
Fapesb and CNPq for the Masters study grant.
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Figure 1. Climate data throughout the year (average temperature,
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flowers of Cambessedesia wurdackii in an area of campo rupestre
vegetation in Mucugê, Bahia State, Brazil. High quality figures are
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Figure 3. Number of visits of Megalopta sodalis and Ptiloglossa aff.
dubia to Cambessedesia wurdackii flowers in relation to the time of
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Figure 4. Relationship between the diameter of the median ocellus
(mm) and head width (mm) of the bees visiting Cambessedesia
wurdackii flowers in an area of campo rupestre vegetation in Mucugê,
Bahia State, Brazil. High quality figures are available online.
Figure 5. Relationship between the ratio of the diameter of the
median ocellus to head width and light intensity (Lux) during the
period of peak bee visits to Cambessedesia wurdackii flowers in an
area of campo rupestre vegetation in Mucugê, Bahia State, Brazil.
High quality figures are available online.
