ABSTRACT INTRODUCTION

1177
Phenology ofBees (Hymenoptera: Apoidea) in a Transition Area
Between the Cerrado and the Amazon Region in Brazil
by
Carlos Alfredo Lopes de Carvalhol, Florisvaldo Mesquita dos Santosl, Rejane
Ferreira Silva2 & Bruno de Almeida Souza3
ABSTRACT
The phenology ofbees in a transition area between the Cerrado and the
Amazon in the Bico-do-Papagaio region, in the State ofTocantins, Brazil,
was studied monthly fram November 1999 to November 2000. The 83 species collected were distributed over the year, and 61.45% occurred in both
the rainy and dry periods, while 19.28% only occurred in the rainy or the dry
period, respectively. The number of individuaIs captured was 54.37% in the
dry period and 45.63% in the rainy period. Bee foraging activity during the
daywas greater in the morning (53.18%), than in the afternoon (46.82%).
The times ofgreater activitywere from 07:01 to 12:00 hours and fram 13:01
to 17:00 hours, particularly during the intervals fram 09:00 to 11 :00 and
from 13:00 to 16:00 hours.
KEYWORDS:
bees
Bico-do-Papagaio
region, seasonal activity, flight activity,
INTRODUCTION
The spatiotemporal abundance patterns of bees on flowers are varied.
Floral density, the phenological synchrany of the activity of adults with plant
blooming and flower anthesis, and the biogeography ofbees and their food
preferences constitute sources of information on the abundance of species
in the habitat (Cane & Payne 1993).
Studies on bee fauna and their associated flora in the Amazon region have
been conducted by different authors, in order to obtain knowledge of the
diversity of species of these insects (Morato & Campos 2000; Santos et aI.
IUniversidade Federal do Recôncavo da Bahia, 44380-000. Cruz das Almas-BA, Brazil.
2lnstituto
Brazil.
de Desenvolvimento
3Escola Superior de Agricultura
Rural do Estado do Tocantins,
"Luiz de ~eiroz",
77000-000, Palmas-TO,
USP, 13418-900. Piracicaba-SP, Brazil.
1178
Sociobiology Vol. 50, No. 3, 2007
2004) and on the flora utilized to collect trophic resources (Absy et aI. 1984;
Carreira & Jardim 1994; Marques-Souza 1996).
The information obtained in this type of study has been more and more
useful in environmental diagnoses. Pollinators and other anthophiles play the
role ofbioindicator organisms; their presence, abundance, and activity can
convey relevant information abolit the status of the environment in which
they are found (Kevan 1999). Another current application is concerned with
their use as a elimatic monitoring too!, since insects are strongly affected by
elimatic variabilities (Gordo & Sanz 2006).
Another research component stilllittle studied in connection with bee
communities in this region is species phenology, in which their foraging
activities are investigated.
The temporal variation in number ofindividuals and species may be related
to the availability of food sources, degree of socialization, multivoltinism of
species, longlife cyeles and intraspecific characteristics (Sakagami et aI. 1967;
Michener 1990). Solitary bee species can decrease their activities during one
or more periods of the year, while eusocial species remain active throughout
the year (Barbola & Laroca 1993; Carvalho 1999).
The objective ofthis studywas to obtain information abolit the community
ofbees and their seasonal activity in a Transition Area between the Cerrado
and the Amazon Region in Brazil.
MATERIAL AND METHODS
Bees were collected every fifteen days in two trails demarcated in the localities ofEsperantina (5° 20' 1" S; 48° 35' 28" W; 118.88m) and Mulatos (5°
20' 28" S; 48° 29' 12"W; 144.94m), between 11/30/1999 and 11/08/2000,
in the municipality ofEsperantina, in the Bico-do-Papagaio region, State of
Tocantins, Brazil. The collected specimens were killed with cotton soaked
in ethyl acetate, previously placed in different containers. Identification was
based on specimens deposited in the Bee Collection of the Entomological
Museum at the Agronomy School ofUniversidade Federal da Bahia, and on
taxonomic keys. Some species were forwarded to specialists. The specimens
were deposited in the Bee Collection ofInstituto de Desenvolvimento Rural
do Estado do Tocantins (Ruraltins) in Palmas-TO; duplicate specimens were
Carvalho, C.A. et aI. - Phenology ofBees 1n a Transition Area in Brazil
1179
donated to the Entomological Museum at UFBA's Agronomy School and to
the specialists who helped with species identification.
Study site characteristics
The region where the study was developed has a hot and humid climate,
characterized by a mean temperature of25°C, with an annual rainfall index
between 1,000-1,800 mm and an annual temperature amplitude between
0.8°C and 3.2°C (Feitosa 1983). The rainfall regime is typically tropical, with
two defined seasons: a rainy season beginning in December and-extending
unti! Apri!, and a dry season, with scattered rains fram May to December.
The typical vegetation in the area is the result of deforestation for the
establishment of pastures and other agricultural activities, and mainly comprises shrubby and herbaceous species, also including ruderal vegetation
elements.
Sampling
The trails, appraximately 1,000 meters in length, were traveled in the period
fram 05:00 to 18:00 hours by two collectors. This route was traveled twice
during the collections (morning and afternoon), tak:ing between 5 and 10
minutes per planto During that period, any bees visiting flowers were captured
with an insect neto
This bee-collectingmethodology,
based on Sakagami et ai. (1967), iswidely
used in similar studies (Barbola & Laraca 1993; Carvalho 1999).
RESULTS AND DISCUSSION
Eighty-three bee species were collected, having their activity distributed
over the study period. Two distinct periods were observed, i.e., the rainy
period between the months ofDecember and April, and the drought period
between May and November (Table 1; Fig. 1).
In the rainy period, the highest number of specimens was collectedin March
(14.33% of total), while in the dry period the months ofJune (13.52%) and
July (13.79%) were important.
The number ofbees collected decreased in the months of April and May,
probably because this is a transition period between the rainy and dry seasons.
?Vloo-VlZ~3713õ'NÕ27x xxx 92distriburion,
xMar
xxxxDec
xx
3862
32 xx õ' 7
Oet
Feb
May
Ju]
Jun
o?~nTable 1.xxxNov
Sep
Apr
Jan
~
Aug
Temporal
'--<
•....•
x
11 xxTotal
63 2000
xxx 1999
3
4 x x 48721 xxx 1
1 Ox xx
1
x 6
x
xx
total number ofindividuals
colleetedxx by 'peeies,
and total
nllmber ofbee species (Hymenoptera:
Apoidea)
in
64 the
a transition arca between
aq
00
•....•
'"
•..... x
5'
1 x xx 451
x
xx
xx
xOct
,.,
:-10
4x
4 xx 12
14
23
x 12000
xxx xx 1999 xxx
xMar
xxxxx
xx
n
I~
73
20
17
73xx xxxx 11
3 xxxx,.,x 49
19
5] xx xTotal
,..,.
10
'"
'<
19
,..,.,
::>
x
xx
Nov
;r
x
x
8
Dec
Feb
Õ
9::>()
xx 6
'"
'"~
<
Jun
2;
~
Jul
Jan
n
Sep
Apr
Table I.May
Aug
Temporal
disrriburion, total number ofindividuals collected
by species,
and total nllmber ofbee speeies (Hymenoptera: Apoidea) in a transition area between the
~
Õ5"
'"
ns::
~.
Cerrado and the Amazon in rhe Bico-do-Papagaio region, State ofTocantins, Brazil: 1999-2000 (conrinlled).
Species
ao
•.....
'"
O
b::I
O
(fQ
b::I
>-;j
"
en rhe
o
00
l'-l
o
õ'
Õ
O
•....•
-...]
?~o
(fq
xxx
xx
xx
xx
xFeb
C/1
ü
xMar
x6
x38
x7 Õ
214
48
351
137
96
31n
5Z
3
Dec
11
22
276
23
29
19
328
318
207
Oct
13
230
333
35
Nov
l'-lxxx xx
763
3115534
253
793
399
748
672
29
Jun
May
Jan
V> 83
Sep
Jul
Apr
Aug
::»
4 xxx'<x 132
3 x
x xx 6
3
xTotal
xx 34
I 2000
xx27
2
xxx 1999 xx 10
133
xx
1
xx
4 x
Cerrado and the Amazon in rhe Bico-do-Papagaio region, State oETocamins, Brazil: 1999-2000 (cominued).
Species
x
x
54
•....•
Carvalho,
C.A. et aI. -
Phenology
ofBees 1n a Transition
Rainy period
'"
'"
a. 62825
45
TI.
10
Z
'"'"
E
Õ
Z
c~00
10
'(3
.~
30
10
.s
300
'"
o
15
150
15
~'"450
350
25
35
100
50
16
§'(3~4Õ'0.~OÓo...~O-;;;
§O 20
200
250
12
Ó
~
40
C
ãi
14
gj O
20
Dry period
____
í"----r- --- -------!
1183
Area in Brazil
oom
_
__
.
._ .m._.
~
i
II
,I
!
!
I
;
I
i
I
i
.
I
I
7i
..j __
l_._..__.._..__
._._.
__ ~
2~
~
O>
oO:O~
~
ªa.z8o
'"
:o
....,
'"O>
....,
u..
';:,
'":::;:
<l:
....,
(f)
52
:::;:
&J
~
Months
Fig. 1. Monthly
between
disrribmion
rhe Cerrado
1999-2000.
:;~oo
'"
<l:
:o
õ
>
of bees, number of plants visited, and precipitation
and rhe Amazon
in the Bico-do-Papagaio
in a transition
region, 5tare ofTocantins,
are a
Brazil:
1184
Sociobiology
Vol. 50, No. 3, 2007
It was observed that after the activity peaks that occurred in the months of
June and July there was a reduction in the number of bees collected, as well
as in the number ofbee species and blooming plams. The smallest amoum
of precipitation in the Bico-do- Papagaio region occurred in the month of
August, which may have influenced the number of blooming pIam species,
direcdy imerfering with bee activity.
Limited periods of availability offood resources, with a consequem reduction in foraging activity, comrasts with the observed need for a permanem
food supply, especially in eusocial bee colonies, in arder to maimain their
populations duringthe food scarcity period (Lorenzon et aI. 2003). Consideringthe distribution ofindividuals collected in the rainy and drought periods, a
certain balance is observed, with a slight advamage during the drought period
(54.37%) (Fig. 2). Similarly, the distribution in number ofbee species was
also balanced, with 19.28% found in each period and 61.45% in both (Fig.
3). Among the species collected, 21 showed eusocial behavior, while the other
species consisted of solitary, parasitic, and primitive social groups.
The variability in social behavior makes it difllcult to imerpret the wide
distribution of individuaIs over the year. In addition, according to Sakagami
et aI. (1967), the phenology is difllcult to establish when individuaIs are dis-
§ Rainy
period K!l Dry period
45.63
54.37
93.09%
6.91 %
Figo 2. Disrriburion
= social species
= solitary species
(%) of rhe number
a transirion area berween rhe Cerrado
Tocantins, Brazil: 1999-2000.
90.69% = social species
9.31 % = solitary species
ofbee
individuaIs
and rhe Amazon
collecred in rhe rainy and dry periods in
in rhe Bico-do-Papagaio
region, Srare of
Carvalho, C.A. et aI. -
Phenology ofBees In a Transition Area in Brazil
1185
tributed throughout the year, since it is influenced by ditlerem factors. This
characteristic is observed particularly in the tropics. According to Michener
(1990), the tropical region may favor the foundation of nests and brood production during all seasons of the year because of mild wimers, According to
Roubik (1989), three to eight generations a year can be produced in tropical,
solitary bee species where adults occur during most of the year.
However, Albuquerque (2001) did not find a relation between climatic
characteristics and the annual activity ofbees in the Baixada
Maranhense
region, State of Maranhão, Brazil, and did not observe clear variation in
abundance of individuaIs and species between the dry and rainy periods. The
decrease in number of collected individuaIs at a given period of the year may
also be associated with the presence of more attractive food sources in the
vicinity of the study area (Pedro 1992).
Another possible explanation for the fact that these groups of bees have
ditlerem distributions over the year has been presemed by Biesmeijer et aI.
(2005) and Biesmeijer & Slaa (2006). According to these aurhors, among
the characteristics of eusocial bees, the presence of activity throughout the
seasons and the exploitation of an ample trophic niche are worth noting,
Consequendy, these bees are considered generalists when compared with
other oligolectic or non-social species.
Despite the difllculties found in imerpretingthe distribution ofindividuals,
several authors have reported on the seasonality ofbees, trying to understand
à.
o Rainy
period O Dry period b::l80th periods
19.28%
Fig. 3. Distribmion (%) of the number of bee species collected in the rainy and dry periods in a
transition area between the Cerrado and the Amazon in the Bico-do-Papagaio region, State of
Tocantins, Brazil: 1999-2000.
1186
Sociobiology Vol. 50, No. 3, 2007
the species dynamics in different ecosystems (Albuquerque
Barros et aI. 2002).
& Rêgo
1989;
In a "caatinga" vegetation of the State ofBahia, Aguiar & Zanella (2005)
observed the occurrence of a higher number of active bee species during the
rainy season when compared to the dry season. They also observed that the
number of active bees was relatively high in the initial part of the dry season,
decreasing in the subsequent months. The opposite situation was observed
in the initial period of the rainy season, possibly because those were transition periods.
In the south of Brazil, Sakagami et aI. (1967) found an intermediate
phenological pattern between temperate and tropical climates. In a study
conducted in a humid tropical climate area of Costa Rica, Heithaus (1979)
observed species of all families throughout the year, although seasonal species
were found to be active either in the dry ar in the wet season.
Aguiar & Martins (1997) studied the phenology ofbees in São João do
Carirí-Paraíba, Brazil, and found a seasonal pattern with greater abundance
of species and individuaIs in the rainy period, with a decrease in the low
precipitation period. In the species Ceblurgus longipalpis, Aguiar & Martins
(1994) observed that adult individuaIs would appear during the rainy season,
in synchrony with the greater abundance of their associated flora.
When the foraging activities ofbees were analyzed througholit the day, it
was observed that 53.18% of the individuaIs were collected in the morning
(05:00 to 12:00hours), while46.82%werecapturedin
theatternoon (12:01 to
18 :00 hours). Albuquerque & Mendonça (1996) observed ahigher frequency
of foraging individuaIs on flowers in the morning during most of the year.
The times with the most activitywere from 07:01 to 12:00 hours in the
morning and from 13:01 to 17:00 hours in the atternoon, with emphasis on
the intervals from 09:00 to 11 :00 and from 13:01 to 16:00 hours. The times
with the least activitywere
from 05:00 to 06:00 and from 17:01 to 18:00
hours (Fig. 4).
There was a progressive reduction in the number of individuaIs collected
in the period from 11:01 to 13:00 hours, which might be associated with
high temperature ar the collection of other resources out of the trail, such as
water (Carvalho 1999).
Carvalho, C.A. et aI. -
Phenology ofBees In a Transirion Area in Brazil
1187
Several authors cited by Pereboom & Biesmeijer (2003) reported that bee
species from tropical and subtrapical regions are subject to high ambient
temperatures and heat production fram flight and foraging activities. This
kind of information has pravided support to several studies, including those
that focus on the life history of bees, foraging ecology, niche division, and
biogeographic distribution patterns of species.
These results are similar to those found by other authors, such as Pedro
(1992), who observed the highest frequency ofindividuals between 10:00
and 14:00 hours, while the lowest frequency was observed between 16:00
and 18:00 hours; Aguiar & Martins (1994), who observed the flower-visiting
activity of C. longipalpis to be about 08:00 hours, extending up to the time
when the flowers remained viable, around 15 :00 hours; and Carvalho (1999),
who observed the greatest flight activity by hourly interval between 09:00
and 10:00 hours and between 13:00 and 14:00 hours.
The reduction in flower visitation throughout the day could be also related
to the etlect of previous visitations made by other bees to those flowers,
~
oN
rá:i
oC;:..:.o?,
'éó
&:i
ái
&:i
r:..:
.9
~
700
300
400
o
500
100
200
O I
600
.z~Õ-o:~-ooc:
,
~
~o
~
,
,
555
Fig. 4. Distribution of rhe number ofbees collecred on flowers by hourly interval in a transirion area
berween rhe Cerrado and rhe Amazon in rhe Bico-do-Papagaio region, 5rare ofTocantins, Brazil:
1999-2000.
1188
Sociobiology Vol. 50, No. 3, 2007
exhausting potential fonts of resources. Thus, WilIiams (1998) cited several
srudies that indicate the rejection of flowers with low nectar reserves by Apis
mellifira and Bombus spp. foragers.
Gonçalves & others (1996) observed that meliponines were more active in
the morning (08:00 to 10:00 hours), whileA. mellifira was more abundant
between 11 :00 and 15:00 hours. The peak activity of Melipona species observed by Sommeijer & others (1983) aiso occurred in the morning, around
08:00 hours, the period with the highest polIen collection intensity.
Ir is important to point out the existence ofvariation in this activitywithin
the same genus, as observed for M asilvai by Souza & others (2006), in which
the peak offlight activityto colIect resources occurred in the period comprised
between 10:01 and 15:00 hours, with polIen colIection concentrated in the
morning. InM scutellaris, however, Pierrot & Schlindwein (2003) observed
greater foraging activity in the first four hours of observation, beginning at
05:00 hours. In addition, this period concentrated 90% of alI polIen colIections made during the day.
Knowledge about this variation in flight activity displayed by various
bee species is important as it generates information that can be used in pollinator management programs and biology srudies, as welI as in studies on
the genetic potential of the colony and on foraging behavior, among others
(Hilário et alo 2000).
ACKNOWLEDGMENTS
The authors thank the Director of the "Instituto de Desenvolvimento Rural
do Estado do Tocantins" - RURAL TINS; the Association ofBeekeepers from
Bico-do- Papagaio region - ABIP A; and the taxonomists J.M.E Camargo and
S.R.M. Pedra (Universidade de São Paulo, Brazil), E.A.B. Almeida and EA.
Silveira (Universidade Federal de Minas Gerais, Brazil), E Zanella (Universidade Federal da Paraíba, Brazil) and G.A.R. Melo (Universidade Federal do
Paraná, Brazil) for the valuable identification of the bees. C.A.L. Carvalho
and B.A. Souza thanks CNPq Research felIowship for partial support.
REFERENCES
Absy, M.L.J.M.F. Camargo, W.E. Kerr
& L.P.A.
Miranda 1984. Espécies de plantas visitadas
por Meliponinae (Hymenoptera, Apoidea), para coleta de pólen na Região do Médio
Amazonas. Rev Bras Biol44: 277-237.
Carvalho, C.A. et aI. Aguiar, C.M.L.
&
C.E Martins
Phenology of Bccs In a Transition Arca in Brazil
1994. Fenologia
longipalpis Urban e Moure, 1993 (Hymenoptera,
Biol9: 125-131.
e preferência
alimentar
Halictidae, Dufoureinae).
1189
de Ceblurgus
Rev Nordest
Aguiar, C.M.L. & C.E Martins 1997. Abundância relativa, diversidade e fenologia de abelhas
(Hymenoptera, Apoidea) na caatinga, São João do Cariri, Paraíba, Brasil. Iheringia Série
Zoologia 83: 151-163.
Aguiar, C.M.L. & EC.v. Zanella 2005. Estrutura de comunidade de abelhas (Hymenoptera:
Apoidea: Apiformis) de uma área na margem do domínio da caatinga (Itatim, BA).
Neotrop Entomol34:
15-24.
Albuquerque, P.M.C., R.G. Ferreira, M.M.C. Rêgo, C.S. Santos & C.M.S. Brito 2001.
Levantamento da fauna de abelhas silvestres (Hymenoptera,
Apoidea) na região da
"baixada maranhense": Vitória do Mearim, MA, Brasil. Acta Amaz 31: 419-430.
lbuquerque, P.M.C., & ].A.C. Mendonça 1996. Anthophoridae
(Hymenoptera:
Bora associada em uma formação de cerrado no município de Barreirinhas,
Acta Amaz 26: 45-54.
Apoidea) e
MA, Brasil.
lbuquerque, P.M.C. & M.M.C. Rêgo 1989. Fenologia das abelhas visitantes de murici
(Brysonima crassiftlia, Malpighiaceae). BoI Mus Para Emilio Goledi Ser Zool 5: 163-
178.
Barbola, 1.E
& S. Laroca
1993. A comunidade
de Apoidea (Hymenoptera)
da Reserva Passa
Dois (Lapa, Paraná, Brasil): L Diversidade, abundância relativa e atividade sazonal. Acta
Biol Paran22: 91-113.
Barros, T.F., C.A.L. Carvalho, N.M. Brito, O.M. Marques,].B.A. Costa, c.F.B. Damasceno,
L.R.C. Passos E.S.P. Santos 2002. Abelhas visitantes de Bores de Pimpinella anisum
L. Magistra 14: 55-60.
Biesmeijer,].C.,E.]. Slaa, M.S. Castro, B.F. Viana,A.M.P. Kleinerr & Y.L. Imperatriz-Fonseca
2005. Connectance ofbrazilian social bee - food plant networks is inBuenced by habitat,
but not by latitude, altitude or network size. Biota Neotfopica 5: 1-9.
Biesmeijer, ].c. & E.]. Slaa 2006. The structure of eusocial bee assemblages
in Brazil.
Apidologie 37: 240-258.
Cane,]. &]. Payne 1993. A regional, annual and seasonal variation in pollinator guilds:
trisect traits ofbees (Hymenoptera, Apoidea) underlie their patterns of abundance at
Vaccinium ashei (Ericaceae). Ann Ent Soc Am 86: 577-588.
Carreira, L.M.M. & M.A.G.Jardim
1994. Análise polínica dos méis de alguns municípios
do estado do Pará. Boi Mus Para Emílio Goeldi Sér Bot 10: 83-89.
Carvalho,
c.A.L.
1999. Diversidade de abelhas (Hymenoptera,
Apoidea) no município
de
Castro Alves-BA [Ph.D Thesis]. Piracicaba (SP): Universidade de São Paulo. 104p.
Feitosa, A.C. 1983. O Maranhão primitivo: uma tentativa de reconstituição.
São Luís,
Augusta. 142p.
Apidae) e
Gonçalves, S.].M., M. Rêgo & A. Araújo 1996. Abelhas sociais (Hymenoptera:
seus recursos Borais em uma região de mata secundária, Alcântara, MA, Brasil. Acta
Amaz 26: 55-68.
1190
Sociobiology Vol. 50, No. 3, 2007
Gordo, O. & J.J. Sanz 2006. Temporal trends in phenology of rhe honey bee Apis mellifera
(L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952-2004). Ecol
Entomol3l:
261-268.
Heithaus, E.R. 1979. Community
structure
of neotropical
flower visiting bees and wasps:
diversity and phenology. Ecology 60: 190-202.
Hilário, S.D., v.L. Imperatriz-Fonseca
& A.M.P. Kleinert 2000. Flight activity and colony
strength in the stingless bee Melipona bicolor bicolor (Apidae, Meliponinae).
Bio160: 299-306.
Kevan, P.G. 1999. Pollinators as bioindicators
of the stare ofthe environment:
Rev Bras
species, activity
and diversity. Agric Ecosyst Environ 74: 373-393.
Lorenzon, M.C.A. C.A.R.Matrangolo
& J.H. Schoereder 2003. Flora visitada pelas abelhas
eussociais (Hymenoptera, Apidae) na Serra da Capivara, em Caatinga do sul do Piauí.
Neotrop Entomol32: 27-36.
Marques-Souza, A.C. 1996. Fontes de pólen exploradas porMelipona compressipes manaosensis
(Apidae: Meliponinae), abelha da Amazônia CentraL Acta Amaz 26: 77-86.
Michener, C.D. 1990. Classification of the Apidae (Hymenoptera).
Univ Kansas Sci Bul
54: 75-164.
Morato, E.E & L.A.O. Campos 2000. Efeitos da fragmentação florestalsobrevespas
solitárias em uma área da Amazônia CentraL Rev Bras Zoo117: 429-444.
Pedro, S.R.M.1992.
Sobre as abelhas (Hymenoptera,
e abelhas
Apoidea) em um ecossistemade cerrado
(Cajuru, NE do Estado de São Paulo): composição, fenologia e visita às flores [MSc.
ThesisJ Ribeirão Preto (SP): Universidade de São Paulo. 200p.
Pereboom, J.J.M.
& J.c.
Biesmeijer 2003. Thermal consrraints
for stingleess bee foragers:
the importance ofbody size and coloration. Oecologia 137: 42-50.
Pierrot, L.M. & C. Schlindwein 2003. Variation on daily flight activity and foragingpatterns
in colonies of uruçu - Melipona scutellaris Latreille (Apidae, Meliponini).
Zoo120: 565-571.
Roubik, D.W. 1989. Ecology and natural history of tropical bees. Cambridge:
University Press, 514p.
Sakagami, S.E, S. Laroca
(PR), South Brazil253-91.
& J.S.
Moure 1967. Wild bees biocenotics
preliminary report. J Fac Sci Hokkaido
Santos, EM., C.A.L. Carvalho
& R.E
Silva 2004. Diversidade
Rev Bras
Cambridge
in São José dos Pinhais
Univ Ser Zoology 19:
de abelhas (Hymenoptera:
Apoidea) em uma área de transição Cerrado-Amazônia.
Acta Amaz 34: 319-328.
Sommeijer, M.]., G.A. Rooy, W. Punt & L.L.M. Bruijn 1983. A comparative studyofforaging
behavior of pollen resources of various stingless bee (Hymenoptera,
Meliponinae)
and honeybees (Hymenoptera, Apidae) in Trindad, West-Indies. Apidologie 14: 205224.
Souza, B.A., c.A.L.
Carvalho
& R.M.O.
Alves 2006. Flight activity of Melipona asilvai
Moure (Hymenoptera: Apidae). BrazJ Bio166: 731-737.
Williams, C.S. 1998. The identity of the previous visitor influences
nectar-collecting
bees. Anim Behav 56: 673-681.
flower rejection
by