Lundiana 4(2):121-124, 2003
© 2003 Instituto de Ciências Biológicas - UFMG
ISSN 1676-6180
Preliminary sampling of Euglossina (Hymenoptera: Apidae:
Apini) of Reserva Particular do Patrimônio Natural “Feliciano
Miguel Abdala”, Caratinga, Minas Gerais, southeastern Brazil
André Nemésio
Laboratório de Sistemática e Ecologia de Abelhas, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas
Gerais. Caixa Postal 486, Belo Horizonte, MG. 30.123-970. Brazil. E-mail: [email protected] or [email protected]
Abstract
Male euglossine bees were attracted to and collected at seven chemical baits in two sites at different distances
from the forest edge at the Reserva Particular do Patrimônio Natural “Feliciano Miguel Abdala”, Caratinga,
Minas Gerais state, southeastern Brazil, a 957 ha remnant of the Atlantic Rain Forest. One hundred twentytwo individuals belonging to seven species were collected. Eulaema cingulata (Fabricius, 1804) was the most
common species at both sites, followed by Euglossa despecta Moure, 1968. β-ionone was the most attractive
bait in both sampling sites, followed by skatole. This study shows that further collections of euglossine bees
at this site are needed.
Keywords: Atlantic Rain Forest, conservation, euglossine bees, Insecta.
Introduction
Euglossina are a Neotropical group of bees occurring from
northern Argentina (Pearson & Dressler, 1985) to southern
United States (Minckley et al., 1996). The males are remarkable
for collecting aromatic compounds at flowers and storing them
in special organs in their posterior tibiae (Dodson et al., 1969),
although the biological function of these compounds is not
fully understood. Euglossina are important pollinators of
several plant species in the families Orchidaceae, Gesneriaceae,
Araceae, Euphorbiaceae, and Solanaceae (Williams, 1982). The
discovery that aromatic compounds were attractive to males and
their artificial synthesis lead to an increase in studies on
composition and seasonality of the local euglossine bee faunas
(e.g. Morato et al., 1992).
Euglossine bee collections have revealed a higher richness
and abundance in Central America and the Amazonian Basin.
However, euglossine collections in the Atlantic Rain Forest are
still sparse and limited in scope. Fewer than a dozen sites have
been studied in this large domain that extends from the state of
Paraíba to Rio Grande do Sul state, eastern Brazil. Several
important remnants of Atlantic Forest have never been sampled
for euglossine bees. Among them, the Reserva Particular do
Patrimônio Natural Feliciano Miguel Abdala (RFMA) is
considered an area of “very high biological importance” for
invertebrate conservation in Minas Gerais state (Silveira, 1998)
Received 21.03.2003
Accepted 25.10.2003
Distributed 30.12.2003
and of very high or extreme biological importance for several
other taxa (e.g. Fonseca & Rylands, 1998; Marini & Lamas,
1998; Silva & Mendonça, 1998; Haddad, 2000).
Despite the importance of euglossine bees as pollinators
and the major biological importance of RFMA in Minas Gerais
state, virtually no data on the euglossine fauna of this area is
available. The aim of this study was to provide a preliminary
inventory of the euglossine fauna of RFMA and compare its
species diversity and abundance among other sites.
Material and Methods
Study Area
The present study was carried out at RFMA (19°43’S 41°49’W), in the municipality of Caratinga, in southeastern Minas Gerais state, near the Manhuaçu river. The reserve covers
957 ha of Tropical Semideciduous Forest, and is included in the
Tropical Atlantic domain (Ab’Saber 1977). The vegetation is in
different stages of regeneration (Hatton et al., 1983) and the
main representative families are: Fabaceae, Rubiaceae,
Asteraceae, Bignoniaceae, and Myrtaceae among phanerogams
(Lombardi & Gonçalves, 2000), and Pteridaceae,
Thelypteridaceae, Tectariaceae, Polypodiaceae, Aspleniaceae,
and Dennstaedtiaceae among pteridophytes (Melo & Salino,
2002).
The climate in the region best fits within Holdridge’s
subtropical humid-subhumid designation (Golfari, 1975),
which is characterized by a dry season, from April to
September, and a rainy season, from October to March (Strier,
1986). Elevations range from 400 to 680 m above sea level
(Silva, 1993).
Nemésio
Sampling
Ten aromatic compounds were tested for their
attractiveness to male euglossine bees: 1,8-cineole, vanillin,
methyl trans-cinnamate, eugenol, benzyl acetate, methyl
salicylate, β−ionone, cresol, skatole, and ρ-tolyl acetate. Two
sites were chosen for collecting bees: one in the interior and
one close to the edge of the forest. A single collection was
carried out at each sampling site, on 1 August 1999, between
10:00-15:00 h. The chemical baits were placed on cotton
waddings hanging from branches at about 1.5 m above the soil
surface and distanced at least 2 m from each other. Bees
attracted to these lures were captured with entomological nets,
killed with ethyl acetate, and separated in labeled envelopes.
The substance to which each bee was attracted and the local
and time it was collected were recorded. All specimens
collected were pinned and are deposited at the Entomological
Collection of the department of zoology of the Universidade
Federal de Minas Gerais. Bees were identified with the aid of
taxonomic keys and by comparison with specimens previously
identified by specialists.
The abundance and richness observed in this study were
compared with those obtained in August, 1999, at three
different areas in Minas Gerais state: nine forest fragments near
Belo Horizonte (19°53’ S, 43°54’ W; elevation: 800-1,100 m),
three sites at Reserva Particular do Patrimônio Natural da Serra
do Caraça (20°05’ S, 43°29’ W; elevation: 800-2,000 m), and
six sites at Parque Estadual do Rio Doce (19º30’ - 19º48’S,
42º30 - 42º36’ W; elevation: 200-500 m) (unpubl. data).
Results
One hundred twenty-two male euglossine bees belonging
to seven species were collected; 59 in the interior of the forest
and 63 at the edge (Tab. 1). Eulaema cingulata (Fabricius,
1804) was the most common species in both areas, representing
37.3% of all collected bees in the interior of the forest and
44.4% at the edge. Euglossa despecta Moure, 1968 was the
second most common species at both sites. Euglossa fimbriata
Rebêlo & Moure, 1995 was only caught at the edge, whereas
Eg. pleosticta Dressler, 1982 occurred exclusively in the interior of the forest.
In both areas, β−ionone was the most attractive bait,
followed by skatole. In the interior of the forest, eugenol was
the third most attractive substance, whereas benzyl acetate was
the third most attractive bait at the forest edge. El. cingulata
was most attracted to β−ionone and skatole in the interior of the
forest, and to benzyl acetate and skatole at the edge. This
species also was attracted to vanillin at the edge, but not in the
interior of the forest. Euglossa despecta was exclusively
attracted to β−ionone. Methyl salicylate, cresol, and ρ-tolyl
acetate were not attractive to male euglossine bees in this study.
At the RPPN Serra do Caraça (RSC) site, only 40
individuals were collected in August 1999; 28 (70.0%) in the
site which presented the highest abundance. At the Belo Horizonte sites (BH), bees were collected in only six of the nine
fragments sampled in August 1999. A total of 177 male
euglossine bees belonging to 10 species were collected at these
six sites. Fifty-six individuals (31.6%) were collected in the
fragment that showed the highest abundance. At Parque
Estadual do Rio Doce (PERD), the largest Atlantic Forest
remnant in Minas Gerais state, 102 male euglossine bees
belonging to nine species were collected at six sampling sites.
Twenty-six individuals (of eight species) was the highest
number recorded for a single site at PERD. The results of the
comparison with other forested areas of Minas Gerais state are
presented in Tab. 2.
Discussion
Comparison of collections at RFMA with those from other
areas in Minas Gerais state suggests a relatively high
abundance of euglossine in RFMA. In Belo Horizonte, only
two sites had a higher richness (nine and eight species) than the
RFMA collections, and all three sites at the RSC had six or
fewer species. Samplings were carried out from 10:00 to 16:00
h in these areas, but only five chemical baits were used
(cineole, vanillin, methyl cinnamate, benzyl acetate, and
eugenol). β-ionone, the most attractive bait in RFMA, was not
used in Belo Horizonte and RSC, but later samplings with this
bait revealed that only Euglossa stellfeldi Moure, 1947 was
attracted to this bait at these sites.
At PERD, collections were carried out from 06:00 to 18:00
h, with 13 chemical baits: the same ten used in this study plus
methyl benzoate, dimethoxybenzene, and β−myrcene.
These data demonstrate that the two sites sampled at
RFMA had the highest average abundance of euglossine bees
out of 20 sites sampled in several regions of Minas Gerais state
in August 1999 (even considering the longer sampling period in
the latter sites). Only two sites in Belo Horizonte region and
one site at PERD had higher richness than RFMA.
Comparison of the richness of RFMA with those of other
long-term inventories in Atlantic Forest remnants shows that
the seven species collected in the present study equals 87.5% of
those observed in northeastern São Paulo state (Rebelo &
Garófalo, 1991), 87.5% of those observed for two fragments in
João Pessoa, Paraíba (Bezerra & Martins, 2001), 70% of the
reported richness for three fragments in Viçosa region, Minas
Gerais state (Peruquetti et al., 1999), 41% of the richness
observed in nine fragments of Belo Horizonte city region, 40%
of the richness of PERD (Nemésio & Silveira, unpubl. data),
and 33% of the richness of Desengano region, Rio de Janeiro
state (Tonhasca Jr. et al., 2002).
In the present study, the attractiveness of cineole was
relatively low. This was the most attractive chemical bait in all
of the studies mentioned above for the Atlantic Forest domain,
and it is also the most attractive bait in other regions (e.g.
Janzen et al., 1982). Two possibilities for this difference are
considered: (i) it is the effect of a single sampling, or (ii) it
merely represents the preferences of the two dominant species
at this area (El. cingulata and Eg. despecta), which were
strongly attracted to β−ionone (Euglossa despecta was
exclusively attracted to this bait). It is important to point out
that this compound has rarely been used in samplings of
euglossine bees and, to date, there is only one report of its use
in Atlantic Forest areas (Peruquetti et al., 1999). The
employment of this bait should be considered in future studies
using the chemical baiting technique.
Given the preliminary data presented in this study, the size
of RFMA, and its biological importance to invertebrates and
Preliminary sampling of Euglossina of Reserva Particular do Patrimônio Natural Feliciano Miguel Abdala
Table 1 -
Specimens of Euglossina collected in the interior of the forest (IF) and at the forest edge (FE) at each chemical bait (C = cineole, V =
vanillin, MC = methyl cinnamate, E = eugenol, BA = benzyl acetate, β = β-ionone, SK = skatole, T = total).
Species
C
V
MC
E
β
BA
SK
T
IF
FE
IF
FE
IF
FE
IF
FE
IF
FE
IF
FE
IF
FE
Eulaema cingulata (Fabricius)
El. nigrita Lepeletier
Euglossa despecta Moure
Eg. securigera Dressler
Eg. truncata Rebêlo & Moure
Eg. pleosticta Dressler
Eg. fimbriata Rebêlo & Moure
–
5
–
–
–
–
–
–
6
–
1
–
–
–
–
–
–
–
–
–
–
4
–
–
–
–
–
–
–
–
–
6
–
–
–
–
–
–
3
–
–
1
–
–
–
5
2
1
–
–
–
–
3
1
–
–
1
–
–
–
–
–
–
11
–
–
–
–
–
–
12
–
13
–
–
–
–
3
–
15
–
–
–
–
9
5
–
–
–
–
–
10
4
–
–
–
–
1
50
20
28
18
3
1
2
Total
5
7
–
4
6
4
8
4
1
11
25
18
14
15
122
Table 2 -
Number of species and specimens of Euglossina collected in four different areas of Minas Gerais state in August, 1999. RFMA = Reserva Particular do Patrimônio Natural Feliciano Miguel Abdala; RSC = Reserva Particular do Patrimônio Natural da Serra do Caraça;
BH = Belo Horizonte region; PERD = Parque Estadual do Rio Doce.
No. species
No. individuals
Sampling sites
RFMA
RSC
BH
PERD
7
122
2
6
40
3
10
177
9
9
102
6
other organisms in this critical region where few Atlantic Forest
remnants remain, a systematic, long-term study of the
euglossine fauna could be of extreme importance.
Acknowledgements
I thank Eduardo M. Veado, director of Estação Biológica
de Caratinga, for allowing the collections of the area, Alexandre Gomes Damasceno, who helped with field work, the Laboratório de Sistemática e Ecologia de Abelhas of the Universidade Federal de Minas Gerais, for logistic support, and Prof.
Fernando Amaral da Silveira, Prof. Elder Ferreira Morato, Flávia Monteiro Coelho, and an anonymous referee for valuable
comments on earlier versions of this manuscript. Benjamin
Bembé helped with Eg. despecta identification. Dr. Jacquelyn
L. Blackmer kindly checked out the English language and made
important comments on the final version of the manuscript.
References
Ab’Saber, A. N. 1977. Os domínios morfo-climáticos na América do Sul. Primeira aproximação. Geomorfologia, 52: 122.
Bezerra, C. P. & Martins, C. F. 2001. Diversidade de
Euglossinae (Hymenoptera, Apidae) em dois fragmentos de
Mata Atlântica localizados na região urbana de João Pessoa,
Paraíba, Brasil. Revista Brasileira de Zoologia, 18: 823835.
Dodson, C. H.; Dressler, R. L.; Hills, G. H.; Adams, R. M. &
Williams, N. H. 1969. Biologically active compounds in
orchid fragrances. Science, 164: 1243-1249.
Fonseca, M. T. & Rylands, A. B. 1998. Mastofauna. In: Costa,
C. M. R.; Herrmann, G.; Martins, C. S.; Lins, L. V. & Lamas, I. R. (Eds.). Biodiversidade em Minas Gerais – Um
atlas para sua conservação. Belo Horizonte, Fundação
Biodiversitas. Pp. 34-36.
Golfari, L. 1975. Zoneamento Ecológico do Estado de Minas
Gerais para Reflorestamento. Série Técnica no 3 do Projeto
de Desenvolvimento e Pesquisa Florestal. Centro de Pesquisa Florestal da Região do Cerrado. Belo Horizonte.
Haddad, C. F. B. 2000. Anfíbios e Répteis. In: Avaliação e
Ações Prioritátias para a Conservação da Biodiversidade
da Mata Atlântica e Campos Sulinos. Ministério do Meio
Ambiente. Conservation International do Brasil, Fundação
SOS Mata Atlântica, Fundação Biodiversitas, Instituto de
Pesquisas Ecológicas, Secretaria do Meio Ambiente do Estado de São Paulo, SEMAD/ Instituto Estadual de Florestas,
MG. Brasília, pp. 19-21.
Hatton, J. N. S. & Thomson, K. 1983. In urgent need of
protection-habitat for the woolly spider monkey. Orix, 18:
24-29.
Janzen, D. H.; DeVries, P. J.; Higgins, M. L. & Kimsey, L. S.
1982. Seasonal and site variation in Costa Rican euglossine
bees at chemical baits in lowland deciduous and evergreen
forests. Ecology, 63: 66-74.
!
Nemésio
Lombardi, J. A. & Gonçalves, M. 2000. Composição florística
de dois remanescentes de Mata Atlântica do sudeste de Minas Gerais, Brasil. Revista Brasileira de Botânica, 23: 255282.
Marini, M. A. & Lamas, I. R. 1998. Avifauna. In: Costa, C. M.
R.; Herrmann, G.; Martins, C. S.; Lins, L. V. & Lamas, I. R.
(Eds.). Biodiversidade em Minas Gerais – Um atlas para
sua conservação. Belo Horizonte, Fundação Biodiversitas.
Pp. 37-39.
Melo, L. C. N. & Salino, A. 2002. Pteridófitas de duas áreas de
floresta da Bacia do Rio Doce no Estado de Minas Gerais,
Brasil. Lundiana, 3: 129-139.
Minckley, R. L. & Reyes, S. G. 1996. Capture of the orchid
bee, Eulaema polychroma (Friese) (Apidae: Euglossini) in
Arizona, with notes on northern distributions of other
mesoamerican bees. Journal of the Kansas Entomological
Society, 69: 102-104.
Morato, E. F.; Campos, L. A. O. & Moure, J. S. 1992. Abelhas
Euglossini (Hymenoptera, Apidae) coletadas na Amazônia
Central. Revista Brasileira de Entomologia, 36: 767-771.
Pearson D. L. & Dressler, R. L. 1985. Two-year study of male
orchid bee (Hymenoptera: Apidae: Euglossini) attraction to
chemical baits in lowland south-eastern Perú. Journal of
Tropical Ecology, 1: 37-54.
Peruquetti, R.C.; Campos, L.A.O.; Coelho, C.D.P.; Abrantes,
C.V.M. & Lisboa, L.C.O. 1999. Abelhas Euglossini
(Apidae) de áreas de Mata Atlântica: abundância, riqueza e
aspectos biológicos. Revista Brasileira de Zoologia, 16
(Supl. 2):101-118.
"
Rebêlo, J. M. M. & Garófalo, C. A. 1991. Diversidade e
sazonalidade de machos de Euglossini (Hymenoptera,
Apidae) e preferência por iscas odores em um fragmento de
floresta no sudeste do Brasil. Revista Brasileira de Biologia, 51: 787-799.
Silva, A. F. & Mendonça, M. P. 1998. Flora. In: Costa, C. M.
R., G. Herrmann, C. S. Martins, L. V. Lins & I. R. Lamas.
Biodiversidade em Minas Gerais – Um atlas para sua
conservação. Fundação Biodiversitas. Belo Horizonte, pp.
49-51.
Silva, L. V. C. 1993. Comparação fitossociológica entre duas
amostragens numa área de clareira em anos consecutivos,
Estação Biológica de Caratinga, MG. Acta Botânica
Brasílica, 7: 119-127.
Silveira, F. A. 1998. Fauna de Invertebrados. In: Costa, C. M.
R.; Herrmann, G.; Martins, C. S.; Lins, L. V. & Lamas, I. R.
(Eds.). Biodiversidade em Minas Gerais – Um atlas para
sua conservação. Belo Horizonte, Fundação Biodiversitas.
Pp. 49-51.
Strier, K. B. 1986. The behavior and ecology of the wooly
spider monkey, or muriqui (Brachyteles arachnoides E.
Geoffroy, 1806). Ph.D. Thesis, Cambridge. University of
Harvard.
Tonhasca Jr., A.; Blackmer, J. L. & Albuquerque, G. S. 2002.
Abundance and diversity of euglossine bees in the
fragmented landscape of the Brazilian Atlantic Forest.
Biotropica, 34: 416-422.
Williams, N. H. 1982. The biology of Orchids and Euglossine
Bees. In: Arditti, J. (Ed.) Orchid Biology: reviews and
perspectives, Ithaca. Cornell University Press, pp. 120-171.