47

Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil
Neotropical Entomology
journal homepage: www.scielo.br/ne
ISSN: 1519-566X
ECOLOGY, BEHAVIOR AND BIONOMICS
Pollen Analysis Reveals Plants Foraged by Africanized Honeybees in the
Southern Pantanal, Brazil
S Borr
1
, CFP Luz
2
, AC Aetuio
3
, A Pott
3
1
Programa de Pós-Graduação em Biologia Vegetal, Univ Federal de Mato Grosso do Sul, Campo Grande, MS, Brasil
2
Secretaria do Meio Ambiente de São Paulo, Insututo de Botânica, Núcleo de Pesquisa em Palinologia, São Paulo, SP, Brasil
3
Depto de Biologia, Univ Federal de Mato Grosso do Sul, Campo Grande, MS, Brasil
Keywords
Apis mellifera, pollen diet, melittophilous
species, pollen trap, wetlands
Correspondence
Stuurt Borr, Programa de Pós-Graduação em
Biologia Vegetal, Univ Federal de Mato Grosso
do Sul, CP 549, 79070-900 Campo Grande,
MS, Brasil. Current address: Programa de Pós-
Graduação em Entomologia FFCLRP-USP, Lab
de Abelhas, Rua do Matão 321, Travessa 14,
05508-090, Insututo de Biociências, USP, São
Paulo, SP, Brasil; samboff@gmail.com
Edited by Angelo Pallini – UFV
Received 10 September 2009 and accepted
05 February 2010
Abstract
The pollen diet of Africanized honeybees Apis mellifera L. was studied
during seven months (October 2006 to April 2007) in a natural forest
fragment in the southern Pantanal, sub-region of Abobral, Mato
Grosso do Sul. The analysis of the pollen diet was based on direct
observations of the bees visiting lowers as well as through the use
of a pollen trap installed in a wild colony in a tree hole in the same
forest fragment. The total of 28 species in 15 botanical families were
observed as potential sources of pollen for A. mellifera, with visits
registered in 24 of these species in 13 botanical families. In the pollen
trap we recorded 25 pollen types. This study is the irst report to use
this type of trap for pollen collection in the Neotropical region and
aimed to identify the polliniferous bee plants of Brazilian pantanal.
Introducton
There has been a differentiation regarding source of
protein during the evolution of Aculeata Hymenoptera
(wasps and bees) (Roubik 1989). Unlike the stinging
wasps which fulill their protein requirements through
predation of other arthropods, bees rely on pollen as
their only protein source (Roubik 1989, Engels 2001).
The pollen is collected at the lowers and transported in
a specialized structure to brood cells in the nest (Roubik
1989, Michener 2007).
In spite of a probable relation between bee choice for
pollen source and the availability of this resource linked
to lower features such as architecture, color and odour,
this preference is still under discussion (Bragavan & Smith
1997, Çakmak et al 1998, Faegri & van der Pijl 1979). In
the case of pollen, the choice of a particular plant species
seems to be related to a set of essential aminoacids
(Pernal & Currie 2002, Cook et al 2003). Pollen grains
are utilized by Apis mellifera L. as protein source to feed
larvae and adults (Zerbo et at 2001), also being essential
for the development of the hypopharyngeal gland of the
nursing bees (Crailsheim 1990).
The composition of pollen loads can vary according to
the region or season, indicating patterns and variations of
the local lora (Barth 2004). Analysis of pollen loads is a
valuable tool for identiication of the origin of apicultural
products (Barth 2005) and can provide data regarding
to the pollen diet of bees (Dimou & Thrasyvoulou
2007). Sampling of pollen loads using traps attached to
natural colonies was done with Trigona collina (Smith)
in Malaysia (Eltz et al 2001) and with A. mellifera in
Europe (Imdorf 1983, Imdorf & Wille 1983). Studies
of pollen diets based on pollen loads usually utilize
48
Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil
Boff et al Pollen Analysis Reveals Plants Foraged by Africanized Honeybees
pollen collectors in Langstroth type hives (Luz et al
2007, Modro et al 2007), direct removal of pollen loads
from the corbicula (Fernandes-da-Silva & Serrão 2000,
Webby 2004), extracted pollen from colony storage pots
(Cortopassi-Laurino & Ramalho 1988, Antonini & Martins
2003) or examination of pollen content in the rectum of
honeybees (Dimou & Thrasyvoulou 2009).
In Brazil, knowledge on the lora visited by bees is
partly empirical and is limited to certain regions (Barth
2004). Many plant species of the Pantanal wetlands are
visited by bees (Pott & Pott, 1999, Pott & Pott unpubl
data), but little is known about the phenology of these
plants, especially in Mato Grosso do Sul (Reis 2003). For
the southern Pantanal region, Pott & Pott (unpubl data)
listed the bee plants by observation of visits (either Apis
or native bees) to lowers, but did not evaluate which
plants were the sources of pollen and/or nectar. The
pantanal of Mato Grosso do Sul presents a wide diversity
of habitats, with predominance of loodable areas, with
herbaceous species more frequent than woody ones (Pott
& Pott 1999). One of the distinct vegetation types are
the natural forested fragments of semideciduous forest,
locally known as “capões”.
Since bees are the main pollinators of angiosperm
species (Michener 2007), the exotic species Apis mellifera
might compete with native bees for resources offered
by these plants (Butz Huryn 1997). Considering the
incentives to expand areas designated to apiculture in
the Pantanal (Reis & Comastri 2003), as well as to the
fact that studies regarding these aspects are scarce, our
objective was to survey the poliniferous lora utilized
by A. mellifera in the pantanal of Mato Grosso do Sul by
carrying ield observations and pollen analysis, and to
test a new technique of pollen trap on a wild colony of
Africanized bees.
Material and Methods
Field observations were performed on the edge of a
natural forested patch (capão) on the Fazenda São Bento
(19° 34’ 36’’S/ 57° 01’ 08’’W), sub-region of Abobral,
township of Corumbá, in the Brazilian pantanal wetland,
Mato Grosso do Sul. The climate is the tropical sub-humid
(“Aw”) as deined by Köppen (1948), with distinct rainy
(October-March) and dry (April-September) seasons.
Average annual rainfall is 1100 mm, and mean annual
temperature is 26°C.
The study was performed between October 2006 and
April 2007, covering one rainy season in a natural forested
patch of 0.62 ha. These forested patches are islets of
woody vegetation generally circular or elliptical in shape,
on a terrain up to 5 m above the loodable grassland. The
vegetation on its edge is lood tolerant, while dry forest
species occur in the interior (Damasceno Jr et al 1999).
The lowering species present at the edge of the
studied forested patch were recorded monthly in four
plots of 5 x 20 m (100 m
2
). Plots were oriented as follows:
one to north, one to south, one to east and one to the
west of the studied forested patch. Only exclusively
polliniferous and polliniferous/nectariferous plants were
recorded in these plots. To obtain data on the probable
pollen diet, direct observations on the honeybees foraging
for pollen in lowers were monthly made in the studied
plots (October 2006 - April 2007). Each lowering species
in a given plot was visually observed for a period of 15
min regarding A. mellifera visits.
In addition, to include in our sample species that
were not registered in the censuses at the studied plots,
we installed a pollen trap attached to the entrance of
a wild colony of A. mellifera in a tree hole inside the
forested patch.Only one pollen trap was included in our
sample since the monitored nest was the only one found
in the forested patchs of the studied area. This trap is a
perforated metal plate with a collector underneath it.
Some holes in the plate had a diameter similar to the
pollen collectors for Langstroth hives (4 mm), retaining
the pollen load of the corbicula; other holes were slightly
larger (5 mm), allowing the bee’s entrance to the hive
with the pollen load. The pollen trap was used for one day
every month, except in the rainy period, when it remained
on the hive for three months (December-February) due
to dificulties of access. The pollen collected in the trap in
this three-month period represented one sample.
The samples of pollen loads were kept in glycerin 50%
and were later analyzed with the classic European method
(Maurizio & Louveaux 1965). Pollen was mixed in 10 ml of
70% ethanol, centrifuged, and the sediment was washed
in distilled water, left for 30 min in 1:1 glycerol:H
2
O, and
centrifuged again. For light microscopy observations,
slides were prepared using glycerin-jelly and sealed with
parafin. The identiication of pollen types was based on
the loristic survey and on pollen catalogues (Salgado-
Labouriau 1973, Roubik & Moreno 1991). A pollen type
is named after an enclosed genus or species, establishing
proximity with a taxonomic group (Salgado-Labouriau
1973, Lorscheitter 1989). For calculation of frequency
classes of each pollen type a total of 300 pollen grains
were counted per sample. Frequency classes were deined
as: dominant pollen (D) > 45% of the total of counted
pollen grains; accessory pollen (A) = 15% to 45%;
important isolated pollen (I) = 3% a 15%; and occasional
isolated pollen (O) < 3% (Zander 1935).
Results
Plants identiied as pollen sources were deined as
lowering species that offered pollen or both nectar
and pollen as resources. During the focal observations
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Boff et al
Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil
Pollen Analysis Reveals Plants Foraged by Africanized Honeybees
and in the vegetation survey a total of 28 species, in
15 families, were observed as pollen sources, with
Malvaceae, Fabaceae and Rubiaceae as the most
representative (Table 1). These plants were mainly
herbs or shrubs, and nine species were exclusively
polliniferous, while 19 species offered both pollen and
nectar (Table 1). Among all these plants, 24 species
were visited by A. mellifera.
A total of 25 types of pollen (Fig 1) were found in
the pollen trap at the entrance of the wild nest (Table
2). The families with the largest number of pollen types
were: Fabaceae (4), Asteraceae (3), Rubiaceae (3),
Euphorbiaceae (2) and Arecaceae (2). Other families were
represented by a single pollen type. Pollen types varied
both in time, frequency and species richness (Table 2).
The highest number of pollen types was recorded (n =
13) during October, followed by December-February,
when the pollen trap was continuously present (n =
10). The other three samples, in November, March and
April, showed lower richness, with six, one and three
pollen types, respectively (Table 2). The Piperaceae
and Scrophulariaceae pollen types had less than three
Table 1 Plant families, species names, potential resource (Res) offered by the plant (p = pollen, n = nectar) and lowering
period from October 2007 to April 2007 for species occurring on the edge of the forest fragment (capão) in southern
pantanal, MS, Brazil.
1
Species in which visits of Apis mellifera were not observed.
Families Species Res
Months
Oct Nov Dec Jan Feb Mar Apr
Alismataceae
Echinodorus paniculatus P+n X
Echinodorus tenellus P X
Asteraceae
Centratherum punctatum P+n X X
Wedelia brachycarpa P+n X X X X
Commelinaceae Commelina erecta P X X X X X
Euphorbiaceae
Croton densiflorus P+n X X
SebasƟania hispida P X X X X X X
Fabaceae
Senna occidentalis
1
P X
Senna spectabilis
1
P X
Senna splendida
1
P X X X X X
Hippocrateaceae Hippocratea volubilis P+n X X X
Lamiaceae HypƟs suaveolens P+n X X X X X X X
Lythraceae Adenaria floribunda P+n X X X X X X
Malvaceae
Melochia parvifolia P+n X X X X X X
Melochia pyramidata P+n X
Melochia simplex P+n X
Sida linifolia P+n X
Sida santaremensis P+n X
Sida viarum P+n X
Onagraceae Ludwigia octovalvis P+n X X
Portulacaceae Portulaca fluvialis P X
Rubiaceae
Psychotria carthagenensis P+n X
Richardia grandiflora P+n X X X X X
Staëlia thymoides P+n X
Salicaceae Casearia aculeata P+n X
Scrophulariacae
Bacopa australis P+n X X
Scoparia montevidensis P X X X X
Solanaceae Solanum viarum
1
P X X X X X
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Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil
Boff et al Pollen Analysis Reveals Plants Foraged by Africanized Honeybees
grains per sample, and were therefore considered to be
contaminants.
Among species which offered exclusively pollen,
Scoparia montevidensis was observed being visited only
by A. mellifera. In addition, lowers adapted for buzz-
pollination, which have poricide anthers, (e.g. Solanum
and Melastomataceae types) were also visited by A.
mellifera. In occasional observations, other exclusively
polliniferous species (e.g. Solanum viarum and Senna
splendida - Table 1) were recorded being visited by
buzz-pollinating bees such as Bombus pauloensis
(Friese), Xylocopa frontalis (Olivier) and Augochloropsis
Fig 1 Light microscopy (LM) pollen micrographs observed in the pollen load samples of wild Africanized Apis mellifera
0n the edge of a forest fragment (capão) in southern Pantanal, MS, Brazil. a-b) Asteraceae. a. Elephantopus; b) Wedelia; c)
Euphorbiaceae; d-e) Fabaceae; d) Mimosa selloi; e) Fabaceae; f) Moraceae, Cecropia; g) Myrtaceae, Myrcia; h) Onagraceae;
i-j) Rubiaceae; i) Richardia; j) Rubiaceae; k) Solanaceae, Solanum. Scale = 10 μm.
10 μ
a
b
l
j k
c
d
e
f
g
h
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Boff et al
Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil
Pollen Analysis Reveals Plants Foraged by Africanized Honeybees
sp. Although Trigona fuscipennis (Friese) is not adapted
for buzz-pollination, it was also observed harvesting
pollen from S. splendida, forcing the anther pores with
its mandibles.
Discussion
Fabaceae, Asteraceae, Rubiaceae, Euphorbiaceae and
Arecaceae are among the families whose lowers were
most used by A. mellifera bees in the area studied. Studies
in areas outside pantanal also reported similar patterns
to those reported here. A survey based on pollen analysis
of pollen loads from A. mellifera and Melipona scutellaris
(Latreille) showed that Arecaceae, Asteraceae, Fabaceae,
Malvaceae, Poaceae and Rubiaceae were among the most
important families for these bees (Carvalho et al 1999,
Ramalho et al 2007). Although the habitats in which these
studies were conducted are quite different from Pantanal,
the results are similar to the present survey. The most
attractive species for honeybees in the present study were
herbs and shrubs, which frequently grow on the edges
of the studied forested patch (Damasceno Jr et al 1999).
Some of the observed species and genera considered
melittophilous had already been indicated as potential
bee plants in pantanal (Araujo & Sazima 2003, Pott & Pott
unpubl data). However, since our study encompassed only
part of the year, the number of bee plants in the forested
patches is probably higher than the number reported
here. In addition, due to the dynamics of the looding
regime in the pantanal wetland, the number of lowering
species can also vary throughout the year (Pott & Pott
unpubl data).
In a study using artiicial lowers, Çakmak et al (1998)
veriied that A. mellifera can concentrate foraging efforts
on a single type of lower, a idelity that is important for
the reproductive success of the involved species, including
cultivated plants (Basualdo et al 2000). As a consequence
of loral idelity during a certain period, almost all the
pollen load of a colony is uniformly derived from a single
species and the proportion of mixed loads can vary from
0 to 3% (Deodikar 1965).
In our study this fact could explain the presence
of Onagraceae as a single pollen type in March. Many
Onagraceae species occur in pantanal, mainly on looded
areas around the forested patchs, remaining until the
soil dries after looding. Therefore, the reported idelity
in the studied area could be related to the scarcity of
other lowering species, due to seasonal inundation of
the loodplain (Pott & Pott 1999). This fact could force
honeybees to visit lowers of a limited number of plants.
Also, loral idelity could be related to the distance
of the hives to loral sources, sometimes being more
advantageous for bees to forage on a single lowering
species that occurs in proximity rather than search for
different lowers (Krebs & Davies 1996). In addition, our
data were gathered from only one nest, and differences
regarding lower resources between hives could occur
(Ramalho et al 2007). Nevertheless, in most of the
sampled months, the bees harvested pollen from different
loral sources. According to Schmidt & Buchmann (1993),
a colony of A. mellifera harvests many plant species, thus
receiving a good nutritional balance that is relected by
the highest richness of the “occasional important” pollen
group found in our study. This is expected when many
Table 2 Dominance of pollen types in pollen loads foraged
by wild Africanized Apis mellifera during seven months from
October 2007 to April 2007 on the edge of a forest fragment
(capão) in the southern pantanal, MS, Brazil.
Frequency classes applied were: dominant pollen (D) ≥ 45%
of the total of counted pollen grains; accessory pollen (A) =
15% to 45%; important isolated pollen (I) = 3% a 15%; and
occasional isolated pollen (O) < 3%.
Pollen type
Months
Oct Nov Dec-feb Mar Apr
Bactris I
Arecaceae I O
Cecropia A A
Elephantopus O A
Wedelia A I O
Sorocea O
Richardia O D I
HypƟs suaveolens O
Euphorbiaceae O I
Myrcia O O
Melastomataceae/
Combretaceae
O
Croton O
Poaceae O
Acacia O
Borreria I I
Sterculiaceae O
Mimosa scabrella I
Alismataceae I
Sapindaceae O
Mimosa selloi A
Asteraceae O
Onagraceae D
Fabaceae A
Solanum A
Rubiaceae A
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Boff et al Pollen Analysis Reveals Plants Foraged by Africanized Honeybees
plant species lower in the same period.
Seasonal variation in collection of pollen by honeybees
could also contribute to the conservation of plant species
in pantanal, if the pollination eficiency of visiting bees
ensures their pollination. On the other hand, if honeybees
are not eficient pollinators, both reproduction of visited
plants and populations of native bees that depend upon
these resources are affected. However, this would mainly
occur with oligoletic bees that are strictly dependent
upon one or a few plant species (Alves dos Santos 2003,
Schlindwein 2004). The plants preferred by oligoletic
bees are mostly herbaceous or shrubs, like the species
of Onagraceae and Asteraceae (Schlindwein 2004), both
recorded as visited by A. mellifera in this study.
Some resources utilized by honeybees were not
observed in the plots, such as Acacia, Arecaceae,
Cecropia, and Myrcia. However, they do occur in the
forested patches (Damasceno Jr et al 1999, Araujo
2001) and have been observed nearby, indicating that
the bees of the monitored nest also gathered resources
in adjacent forested patchs. The analysis of pollen loads
also allowed us to conclude that certain plants known
for supplying nectar, also offer pollen to A. mellifera (e.g.
Wedelia brachycarpa). This also indicates that the trap
used for pollen sampling is an eficient method to study
pollen diet of bees in natural colonies. The observed
pollen types in the pollen loads collected in the trap are
to be considered typical of the habitats and vegetation
forms of the study area (natural forested islands and
herbaceous surroundings), allowing the identiication of
the loral origin of the pollen supply during the analyzed
period. Apis mellifera fed mainly on herbs and shrubs, the
predominant growth habit of species occurring on the
edges of the forested patchs, as well as in the loodable
grasslands. Meanwhile, these bees also forage on lowers
of trees and lianas, mainly during the beginning of the
wet period in October-November.
The physiognomy of pantanal wetlands composed
of open grasslands with forested areas restricted to the
natural forested patchs, ancient levee and gallery forests
(Pott & Pott 2004) favors the expansion of populations of
Africanized honeybees (Gonçalves 1994). A fundamental
aspect to be focused in future research regarding
conservation in pantanal is the relation between the
fauna of native bees and plants they pollinate, analyzing
the effects of the presence of A. mellifera on this process.
An alternative proposal is meliponiculture, which is
the management of colonies of native stingless bees.
This activity is important also for the development of
human local communities, being an economic alternative
(Cortopassi-Laurino et al 2006).
In conclusion, our data support an apicultural
calendar for the Abobral sub-region. However, we
suggest that the evaluation of the lora of the pantanal
as pollen resource for A. mellifera should include a larger
number of the forested patches and landscapes, as well
as year-round studies, since species richness tends to
increase with sample size. Finally, Apis mellifera feeding
on the same lower resources as the native bees may
be a possible competitor. Hence, intensive apiculture
in this environment should be thoroughly discussed,
evaluating the hypothesis of resource overlap between
A. mellifera and native bees, as well as verifying the effect
of pollination by honeybees on the reproductive success
of the native plants of the pantanal wetland. Studies
comparing pollination eficiencies of native bees and
honeybees, focusing on the number of fruits and seeds
produced by plant species recorded here, as well as
monitoring nests of native bees are encouraged.
Acknowledgments
To Roberto, riverside dweller of the Miranda river, and
Ana Neves for help in the ield. To Ângela Maria da Silva
Corrêa for assistance with pollen identiication and to
Priscila Rodrigues for help with mounting laminae. To
the University of Mato Grosso do Sul (UFMS) for logistic
support. To PROPP/UFMS for providing funds for English
revision. To Capes/ Fundect-MS for the grant given to the
irst author.
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left for 30 min in 1:1 glycerol:H2O. and centrifuged again. with distinct rainy (October-March) and dry (April-September) seasons. locally known as “capões”. mellifera visits. This trap is a perforated metal plate with a collector underneath it. the exotic species Apis mellifera might compete with native bees for resources offered by these plants (Butz Huryn 1997). 1999. but did not evaluate which plants were the sources of pollen and/or nectar. In Brazil. on a terrain up to 5 m above the loodable grassland. centrifuged. A pollen type is named after an enclosed genus or species. retaining the pollen load of the corbicula. township of Corumbá. Modro et al 2007). During the focal observations 48 Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil . mellifera in the pantanal of Mato Grosso do Sul by carrying ield observations and pollen analysis. direct observations on the honeybees foraging for pollen in lowers were monthly made in the studied plots (October 2006 . direct removal of pollen loads from the corbicula (Fernandes-da-Silva & Serrão 2000. one to east and one to the west of the studied forested patch. The pollen collected in the trap in this three-month period represented one sample. The pollen trap was used for one day every month. Each lowering species in a given plot was visually observed for a period of 15 min regarding A. Since bees are the main pollinators of angiosperm species (Michener 2007). especially in Mato Grosso do Sul (Reis 2003).Pollen Analysis Reveals Plants Foraged by Africanized Honeybees Boff et al pollen collectors in Langstroth type hives (Luz et al 2007. to include in our sample species that were not registered in the censuses at the studied plots. and the sediment was washed in distilled water. Pott & Pott unpubl data).62 ha. Only exclusively polliniferous and polliniferous/nectariferous plants were recorded in these plots. Pollen was mixed in 10 ml of 70% ethanol. For light microscopy observations. extracted pollen from colony storage pots (Cortopassi-Laurino & Ramalho 1988. Lorscheitter 1989).April 2007). The study was performed between October 2006 and April 2007. other holes were slightly larger (5 mm). when it remained on the hive for three months (December-February) due to dif iculties of access. covering one rainy season in a natural forested patch of 0. with predominance of loodable areas. but little is known about the phenology of these plants. with herbaceous species more frequent than woody ones (Pott & Pott 1999). Average annual rainfall is 1100 mm. These forested patches are islets of woody vegetation generally circular or elliptical in shape. while dry forest species occur in the interior (Damasceno Jr et al 1999). The identi ication of pollen types was based on the loristic survey and on pollen catalogues (SalgadoLabouriau 1973. For calculation of frequency classes of each pollen type a total of 300 pollen grains were counted per sample. Considering the incentives to expand areas designated to apiculture in the Pantanal (Reis & Comastri 2003). Material and Methods Field observations were performed on the edge of a natural forested patch (capão) on the Fazenda São Bento (19° 34’ 36’’S/ 57° 01’ 08’’W). important isolated pollen (I) = 3% a 15%. In addition. For the southern Pantanal region. except in the rainy period. Webby 2004). accessory pollen (A) = 15% to 45%. establishing proximity with a taxonomic group (Salgado-Labouriau 1973. one to south. Antonini & Martins 2003) or examination of pollen content in the rectum of honeybees (Dimou & Thrasyvoulou 2009). One of the distinct vegetation types are the natural forested fragments of semideciduous forest. sub-region of Abobral. in the Brazilian pantanal wetland.Only one pollen trap was included in our sample since the monitored nest was the only one found in the forested patchs of the studied area. Plots were oriented as follows: one to north. The samples of pollen loads were kept in glycerin 50% and were later analyzed with the classic European method (Maurizio & Louveaux 1965). The vegetation on its edge is lood tolerant. The pantanal of Mato Grosso do Sul presents a wide diversity of habitats. Mato Grosso do Sul. and to test a new technique of pollen trap on a wild colony of Africanized bees. The climate is the tropical sub-humid (“Aw”) as de ined by Köppen (1948). To obtain data on the probable pollen diet. and occasional isolated pollen (O) < 3% (Zander 1935). our objective was to survey the poliniferous lora utilized by A. allowing the bee’s entrance to the hive with the pollen load. Some holes in the plate had a diameter similar to the pollen collectors for Langstroth hives (4 mm). Roubik & Moreno 1991). Pott & Pott (unpubl data) listed the bee plants by observation of visits (either Apis or native bees) to lowers. knowledge on the lora visited by bees is partly empirical and is limited to certain regions (Barth 2004). slides were prepared using glycerin-jelly and sealed with paraf in. as well as to the fact that studies regarding these aspects are scarce. Many plant species of the Pantanal wetlands are visited by bees (Pott & Pott. Results Plants identi ied as pollen sources were de ined as lowering species that offered pollen or both nectar and pollen as resources. and mean annual temperature is 26°C. mellifera in a tree hole inside the forested patch. The lowering species present at the edge of the studied forested patch were recorded monthly in four plots of 5 x 20 m (100 m2). Frequency classes were de ined as: dominant pollen (D) > 45% of the total of counted pollen grains. we installed a pollen trap attached to the entrance of a wild colony of A.

while 19 species offered both pollen and nectar (Table 1). These plants were mainly herbs or shrubs. and nine species were exclusively polliniferous. Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil 49 . potential resource (Res) offered by the plant (p = pollen. Other families were represented by a single pollen type. The highest number of pollen types was recorded (n = 13) during October. when the pollen trap was continuously present (n = 10).Boff et al Pollen Analysis Reveals Plants Foraged by Africanized Honeybees and in the vegetation survey a total of 28 species. were observed as pollen sources. Asteraceae (3). in 15 families. Among all these plants. The other three samples. species names. with Malvaceae. n = nectar) and lowering period from October 2007 to April 2007 for species occurring on the edge of the forest fragment (capão) in southern pantanal. MS. Fabaceae and Rubiaceae as the most representative (Table 1). respectively (Table 2). frequency and species richness (Table 2). A total of 25 types of pollen (Fig 1) were found in the pollen trap at the entrance of the wild nest (Table 2). in November. March and April. The families with the largest number of pollen types were: Fabaceae (4). followed by December-February. Families Alismataceae Asteraceae Commelinaceae Euphorbiaceae Species Echinodorus paniculatus Echinodorus tenellus Centratherum punctatum Wedelia brachycarpa Commelina erecta Croton densiflorus Sebas ania hispida Senna occidentalis Fabaceae Hippocrateaceae Lamiaceae Lythraceae Senna spectabilis Senna splendida 1 1 1 Res P+n P P+n P+n P P+n P P P P P+n P+n P+n P+n P+n P+n P+n P+n P+n P+n P P+n P+n P+n P+n P+n P P Months Oct Nov Dec Jan Feb X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X Mar Apr Hippocratea volubilis Hyp s suaveolens Adenaria floribunda Melochia parvifolia Melochia pyramidata Melochia simplex Sida linifolia Sida santaremensis Sida viarum Malvaceae Onagraceae Portulacaceae Rubiaceae Salicaceae Scrophulariacae Solanaceae 1 Ludwigia octovalvis Portulaca fluvialis Psychotria carthagenensis Richardia grandiflora Staëlia thymoides Casearia aculeata Bacopa australis Scoparia montevidensis Solanum viarum 1 Species in which visits of Apis mellifera were not observed. showed lower richness. The Piperaceae and Scrophulariaceae pollen types had less than three Table 1 Plant families. with six. 24 species were visited by A. Rubiaceae (3). Pollen types varied both in time. one and three pollen types. Brazil. mellifera. Euphorbiaceae (2) and Arecaceae (2).

other exclusively polliniferous species (e.g. b) Wedelia. (e. Scale = 10 μm. f) Moraceae. In addition. Myrcia. j) Rubiaceae. Solanum and Melastomataceae types) were also visited by A. i-j) Rubiaceae. mellifera. g) Myrtaceae. a. lowers adapted for buzzpollination. In occasional observations. Brazil.Table 1) were recorded being visited by buzz-pollinating bees such as Bombus pauloensis (Friese).g. Solanum. MS. d-e) Fabaceae.Pollen Analysis Reveals Plants Foraged by Africanized Honeybees Boff et al c b a 10 μ d e f l g h j k Fig 1 Light microscopy (LM) pollen micrographs observed in the pollen load samples of wild Africanized Apis mellifera 0n the edge of a forest fragment (capão) in southern Pantanal. mellifera. Cecropia. Xylocopa frontalis (Olivier) and Augochloropsis 50 Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil . e) Fabaceae. Elephantopus. d) Mimosa selloi. c) Euphorbiaceae. which have poricide anthers. k) Solanaceae. grains per sample. Among species which offered exclusively pollen. a-b) Asteraceae. h) Onagraceae. Solanum viarum and Senna splendida . i) Richardia. Scoparia montevidensis was observed being visited only by A. and were therefore considered to be contaminants.

Discussion Fabaceae. mellifera and Melipona scutellaris (Latreille) showed that Arecaceae. including cultivated plants (Basualdo et al 2000). accessory pollen (A) = 15% to 45%. In addition. Many Onagraceae species occur in pantanal. Asteraceae. In a study using arti icial lowers. a idelity that is important for the reproductive success of the involved species. remaining until the soil dries after looding. Pott & Pott unpubl data). Fabaceae. forcing the anther pores with its mandibles. However. almost all the pollen load of a colony is uniformly derived from a single species and the proportion of mixed loads can vary from 0 to 3% (Deodikar 1965). our data were gathered from only one nest. mellifera harvests many plant species. Therefore. which frequently grow on the edges of the studied forested patch (Damasceno Jr et al 1999). mainly on looded areas around the forested patchs. since our study encompassed only part of the year. In our study this fact could explain the presence of Onagraceae as a single pollen type in March. This fact could force honeybees to visit lowers of a limited number of plants. Euphorbiaceae and Arecaceae are among the families whose lowers were most used by A. mellifera can concentrate foraging efforts on a single type of lower. due to seasonal inundation of the loodplain (Pott & Pott 1999). the results are similar to the present survey. thus receiving a good nutritional balance that is re lected by the highest richness of the “occasional important” pollen group found in our study. loral idelity could be related to the distance of the hives to loral sources. and occasional isolated pollen (O) < 3%. important isolated pollen (I) = 3% a 15%. Poaceae and Rubiaceae were among the most important families for these bees (Carvalho et al 1999. Malvaceae. Nevertheless. Although Trigona fuscipennis (Friese) is not adapted for buzz-pollination. sometimes being more advantageous for bees to forage on a single lowering species that occurs in proximity rather than search for different lowers (Krebs & Davies 1996). sp. As a consequence of loral idelity during a certain period. Çakmak et al (1998) veri ied that A. Asteraceae. According to Schmidt & Buchmann (1993). the number of bee plants in the forested patches is probably higher than the number reported here. Studies in areas outside pantanal also reported similar patterns to those reported here. A survey based on pollen analysis of pollen loads from A. MS. the reported idelity in the studied area could be related to the scarcity of other lowering species. and differences regarding lower resources between hives could occur (Ramalho et al 2007).Boff et al Pollen Analysis Reveals Plants Foraged by Africanized Honeybees Table 2 Dominance of pollen types in pollen loads foraged by wild Africanized Apis mellifera during seven months from October 2007 to April 2007 on the edge of a forest fragment (capão) in the southern pantanal. it was also observed harvesting pollen from S. In addition. Pollen type Bactris Arecaceae Cecropia Elephantopus Wedelia Sorocea Richardia Hyp s suaveolens Euphorbiaceae Myrcia Melastomataceae/ Combretaceae Croton Poaceae Acacia Borreria Sterculiaceae Mimosa scabrella Alismataceae Sapindaceae Mimosa selloi Asteraceae Onagraceae Fabaceae Solanum Rubiaceae Months Oct I I A O A O O O O O O O O O I I O I I O A O D A A A I O D I I A A O O Nov Dec-feb Mar Apr Frequency classes applied were: dominant pollen (D) ≥ 45% of the total of counted pollen grains. Ramalho et al 2007). Brazil. Although the habitats in which these studies were conducted are quite different from Pantanal. mellifera bees in the area studied. the number of lowering species can also vary throughout the year (Pott & Pott unpubl data). Also. the bees harvested pollen from different loral sources. Rubiaceae. The most attractive species for honeybees in the present study were herbs and shrubs. splendida. This is expected when many Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil 51 . in most of the sampled months. due to the dynamics of the looding regime in the pantanal wetland. a colony of A. Some of the observed species and genera considered melittophilous had already been indicated as potential bee plants in pantanal (Araujo & Sazima 2003.

Acknowledgments To Roberto. Barth OM (2004) Melissopalynology in Brazil: a review of pollen analysis of honeys. evaluating the hypothesis of resource overlap between A. Araujo AC. such as Acacia. Bedascarrasbure E. Apis mellifera fed mainly on herbs and shrubs. Schlindwein 2004). Arecaceae. focusing on the number of fruits and seeds produced by plant species recorded here. Barth OM (2005) Botanical resources used by Apis mellifera determined by pollen analysis of royal jelly in Minas Gerais. both reproduction of visited plants and populations of native bees that depend upon these resources are affected. De Jong D (2000) Africanized honeybees (Hymenoptera: Apidae) have a greater idelity to sun lowers than European honey bees. as well as monitoring nests of native bees are encouraged. Hence. Smith BH (1997) Olfactory conditioning in the honey 52 Neotrop Entomol 40(1): 47-54 © 2011 Sociedade Entomológica do Brasil . PhD thesis. Araujo. Apis mellifera feeding on the same lower resources as the native bees may be a possible competitor.Pollen Analysis Reveals Plants Foraged by Africanized Honeybees Boff et al plant species lower in the same period. To the University of Mato Grosso do Sul (UFMS) for logistic support. since species richness tends to increase with sample size. indicating that the bees of the monitored nest also gathered resources in adjacent forested patchs. This activity is important also for the development of human local communities. we suggest that the evaluation of the lora of the pantanal as pollen resource for A. Wedelia brachycarpa). Araujo 2001) and have been observed nearby. if honeybees are not ef icient pollinators. like the species of Onagraceae and Asteraceae (Schlindwein 2004). Antonini Y. Brazil. On the other hand. The physiognomy of pantanal wetlands composed of open grasslands with forested areas restricted to the natural forested patchs. Alves-dos-Santos I Apoidea Neotropica: homenagem aos 90 anos de Jesus Santiago Moure. The analysis of pollen loads also allowed us to conclude that certain plants known for supplying nectar. However. Brazil. Seasonal variation in collection of pollen by honeybees could also contribute to the conservation of plant species in pantanal. intensive apiculture in this environment should be thoroughly discussed. Martins RP (2003) The value of a tree species (Caryocar brasiliense) for a stingless bee Melipona quadrifasciata quadrifasciata. and Ana Neves for help in the ield. this would mainly occur with oligoletic bees that are strictly dependent upon one or a few plant species (Alves dos Santos 2003. as well as in the loodable grasslands. The observed pollen types in the pollen loads collected in the trap are to be considered typical of the habitats and vegetation forms of the study area (natural forested islands and herbaceous surroundings). both recorded as visited by A. The plants preferred by oligoletic bees are mostly herbaceous or shrubs. This also indicates that the trap used for pollen sampling is an ef icient method to study pollen diet of bees in natural colonies. In conclusion. However. riverside dweller of the Miranda river. also offer pollen to A. analyzing the effects of the presence of A. as well as year-round studies. mellifera (e. Universidade Estadual de Campinas. Flora (Jena) 198: 427-435. mellifera should include a larger number of the forested patches and landscapes. Sci Agric 61: 342-350. which is the management of colonies of native stingless bees. Cecropia. J Econ Entomol 93: 304-307. To Capes/ Fundect-MS for the grant given to the irst author. and Myrcia. Studies comparing pollination ef iciencies of native bees and honeybees. To PROPP/UFMS for providing funds for English revision. AC (2001) Flora. Sazima M (2003) The assemblage of lowers visited by hummingbirds in the “capões” of Southern Pantanal. being an economic alternative (Cortopassi-Laurino et al 2006). ancient levee and gallery forests (Pott & Pott 2004) favors the expansion of populations of Africanized honeybees (Gonçalves 1994). if the pollination ef iciency of visiting bees ensures their pollination. Editora UNESC. our data support an apicultural calendar for the Abobral sub-region. 109p. Finally. mainly during the beginning of the wet period in October-November. Bragavan S. In Melo GAR. propolis and pollen loads of bees. A fundamental aspect to be focused in future research regarding conservation in pantanal is the relation between the fauna of native bees and plants they pollinate. References Alves-dos-Santos I (2003) Adaptations of bee proboscides for collecting pollen from Pontederiaceae lowers. Mato Grosso do Sul. mellifera in this study. Basualdo M. 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