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Author's personal copy

Journal of Arid Environments 74 (2010) 1355e1358

Contents lists available at ScienceDirect

Journal of Arid Environments

journal homepage: www.elsevier.com/locate/jaridenv

Short Communication

Bee pollen loads and their use in indicating owering in the Caatinga region
of Brazil
Jalson Santos de Novais a, *,1, Luciene Cristina Lima e Lima b, Francisco de Assis Ribeiro dos Santos a
a

Laboratrio de Micromorfologia Vegetal, Programa de Ps-Graduao em Botnica, Universidade Estadual de Feira de Santana, Av. Transnordestina,
s/n, Novo Horizonte, 44036-900 Feira de Santana, Bahia, Brazil
b
Laboratrio de Estudos Palinolgicos, Departamento de Cincias Exatas e da Terra, Universidade do Estado da Bahia, Campus II, Caixa Postal 59,
48040-210 Alagoinhas, Bahia, Brazil

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 25 January 2010
Received in revised form
6 May 2010
Accepted 7 May 2010
Available online 2 June 2010

The study presents a map of pollen samples collected by Apis mellifera L. in an area of Caatinga (dryland)
vegetation in Canudos, Bahia State, Brazil. A total of 62 bee pollen samples obtained from pollen-traps
between March/2004 and February/2006 were examined. The pollen loads were acetolyzed and the
pollen types identied and counted by sampling using an optical microscope. Thirty-six plant families
were found to contribute to the composition of the pollen spectrum of the samples, with 85 different
pollen types. Fabaceae was the most represented family (21 pollen types), and Mimosa lipes was the
single most frequently observed pollen type (37 samples). The predominant pollen class included 14
pollen types; the secondary class, 18 types; important minor class, 37 types; minor class, 38 types; and 37
present pollen types (<1%). Plant species characteristic of the Caatinga region that have apicultural
potential, such as Croton spp., Spondias tuberosa Arruda and Ziziphus joazeiro Mart., were well represented in the pollen spectrum. The pollen map was found to be useful for indicating the owering
periods of certain Caatinga species if long and continuous observations were made.
2010 Elsevier Ltd. All rights reserved.

Keywords:
Apis mellifera
Beekeeping
Melissopalynology
Phenology
Pollen spectrum
Semi-arid

1. Introduction
Pollen is a vital product for bees, principally due to its critical
role in the diet of their larvae (Wiese, 1985). Plants contribute
greatly to the sustenance of these insects, and they are in turn of
notable importance in the pollination and reproduction of many
plant groups (Simpson and Neff, 1983).
Apis mellifera L. is a very successful bee species due to its
capacity to adapt to diverse environments and to out-compete
many species of native bees. Since the 1950s, honeybees have been
introduced into (and raised in) the entire Brazil, including the dry
northeast region (Santos, 2006).
Studies of the pollen loads of A. mellifera have contributed to
a systematized characterization of the apicultural ora in many
countries, and have been especially useful in providing information

* Corresponding author. Tel.: 55 75 3224 8238; fax: 55 75 3224 8132.

E-mail addresses: novais.js@gmail.com (J. Santos de Novais), llima@gd.com.br
(L.C. Lima e Lima), fasantos@uefs.br (F. de A. Ribeiro dos Santos).
1
Present address: Centro de Formao Interdisciplinar, Universidade Federal do
Oeste do Par, Av. Marechal Rondon, s/n, Caranazal, 68060-070 Santarm, Par,
Brazil.
0140-1963/$ e see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jaridenv.2010.05.005

to beekeepers (Biesmeijer et al., 1992; Webby, 2004; Andrada and

Tellera, 2005; Dimou and Thrasyvoulou, 2007). Studies of this
type are still few in Brazil and are still far from being able to furnish
detailed information about the diversity and potential of the native
apicultural ora (Carvalho et al., 1999; Marchini et al., 2000; Novais
et al., 2009).
Activities such as apiculture and meliponiculture have an
important role in the subsistence economies of many localities in
the semi-arid region of Brazil, and these activities contribute to
sustainable regional development by using resources naturally
supplied by the ora and fauna characteristic of the Caatinga
biome. As such, melissopalynological studies can offer valuable
information about apiculture and meliponiculture products
(mainly valuable in terms of exportation markets) as they can
indicate botanical and geographical origin of the products (Santos,
2006; Oliveira et al., 2010).
This study presents a pollen map of the pollen loads transported
by Africanized honeybees in an area of Caatinga vegetation in
northeastern Brazil. Additionally, as the pollen spectrum of
apiculture products reects the ora available to the bees, we
investigated the usefulness of this pollen data in providing information about the owering of plants utilized by these insects in the
study area.

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1356

J. Santos de Novais et al. / Journal of Arid Environments 74 (2010) 1355e1358

2. Material and methods

2.1. Study area
The Canudos Biological Station (CBS) is managed by the Fundao Biodiversitas, and it is located in the municipality of Canudos
in the northeastern micro-region of Bahia State, Brazil (09 540 S,
39 070 W, altitude: 400 m). The CBS experiences average annual
temperatures of 24.15  C, with November through March being the
warmest season of the year and the period of greatest rainfall,
although annual precipitation usually amounts to less than
400 mm (SEI, 1998).
The vegetation in the CBS is predominantly composed of
shrubby hyperxerophytic Caatinga whose oristic composition has
a high level of endemism in comparison to most Caatinga areas
(Silva, 2007).
2.2. Obtaining and analyzing bee pollen samples
Sixty-two bee pollen samples were collected between March/
2004 and February/2006 from colonies of A. mellifera installed in
the study area. The pollen-traps were placed at the entrances of the
hives by a 24-h period, starting at 18.00 h. The samples were processed in the Plant Micromorphology Laboratory (LAMIV) of the
Universidade Estadual de Feira de Santana (UEFS), Feira de Santana,
Bahia State, Brazil.
The samples were prepared by dehydrating the pollen loads in
a drying oven at 40  C until attaining a constant weight and were
subsequently processed using the methodology of Alvarado and
Delgado (1985), with modications described by Novais et al.

(2009). The pollen sediments were acetolyzed according to the

procedures described by Erdtman (1960).
Each acetolyzed sample was mounted in glycerin jelly on four or
more slides; one preparation was mounted in glycerin jelly stained
with safranin. All of the slides were subsequently deposited in the
LAMIV/UEFS pollen library.
After identifying the pollen types present on the slides, at least
1200 pollen grains were counted using sampling methods to
establish the occurrence percentages of each pollen type:
Predominant Pollen -PP (>45%), Secondary Pollen -SP (16e45%),
Important Minor Pollen -IP (3e15%), Minor Pollen -MP (1e2%), and
Present (<1%) (Louveaux et al., 1978).
Considering only the presence or absence of a given pollen type
in the samples, we adopted the following constancy classes: Very
Constant (present in >75% of the samples), Constant (>50e75%),
Low Constant (>25e50%), Occasional (e25%) and Rare (<5%)
(Novais et al., 2009).
Pollen library samples at LAMIV, as well as palynological reference catalogs were used to determine the botanical afnity of the
pollen types.
Information concerning the owering of some of the species at
the CBS was obtained during monthly surveys in 2004 by Silva
(2007) and is presented here and compared to the pollen data
gathered from the hives.
3. Results
A total of 85 different pollen types were identied in the samples,
with the best represented families being: Fabaceae (21 pollen types:
Caesalpinioideae, 10; Mimosoideae, 8; Papilionoideae, 3), Asteraceae,

Fig. 1. Some pollen types found in bee-collected pollen loads from Canudos, Bahia State, Brazil. Aca: Angelonia campestris, Aco: Anadenanthera colubrina, C: Croton, Cm: Caesalpinia
microphylla, Cp: Conocliniopsis prasiifolia, Dr: Diodia radula, Jr: Jatropha ribifolia, Le: Lippia elegans, Mb: Mitracarpus baturitensis, Mm: Mimosa misera, Pj: Prosopis juliora, Pr: Plathymenia reticulata, Re: Rhaphiodon echinus, Tm: Turnera melochioides, Vs: Vernonanthura subverticillata and, Z: Zornia. Scale bars 30 mm.

Author's personal copy

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Molluginaceae
Poaceae
Poaceae
Rubiaceae
Scrophulariaceae
Verbenaceae

Krameriaceae
Lamiaceae
Malvaceae s.l.

Fabaceae

Euphorbiaceae

Alternanthera ramosissima (Mart.) Chodat

Conocliniopsis prasiifolia (DC.) R.M.King & H.Rob.
Commiphora leptophloeos (Mart.) J.B.Gillett
Melocactus zehntneri (Britton & Rose) Luetzelb.
Pilosocereus tuberculatus (Werderm.)
Byles & G.D.Rowley
Jatropha ribifolia (Pohl) Baill.
Croton sp.
Cratylia mollis Mart. ex Benth.
Mimosa lewisii Barneby
Poincianella microphylla (Mart. ex G.Don)
L.P.Queiroz
Krameria tomentosa A. St.-Hil.
Hypenia salzmannii (Benth.) Harley
Herissantia tiubae (K. Schum.) Brizicky
Melochia tomentosa L.
Sida sp.
Mollugo verticillata L.
Digitaria tenuis Henrard
Trachypogon spicatus Kuntze
Mitracarpus baturitensis Sucre
Angelonia campestris Nees & Mart.
Lippia thymoides Mart. & Schauer

J
Plant species

Pollen types of the family Fabaceae have occurred very

frequently in pollen analyses undertaken in semi-arid regions in
Brazil and demonstrated the importance of this plant group to
Africanized honeybees (Sodr et al., 2007; Novais et al., 2009),
eusocial native bees (Novais et al., 2006), and solitary species
(Drea et al., 2009).
Among the Fabaceae, the genus Mimosa is very important for
providing oral resources to bees. According to biogeographical
data of Queiroz (2009), the genus Mimosa is well represented in dry
regions and has the greatest diversity among the different Fabaceae
genera found in Caatinga areas. Mimosa arenosa (Willd.) Poir. var.
arenosa, M. lipes Mart., M. lewisii Barneby, and M. misera Benth.,

Amaranthaceae
Asteraceae
Burseraceae
Cactaceae

4. Discussion

1357

Family

Euphorbiaceae, Malvaceae s.l. and Rubiaceae (ve types each), Poaceae (four), Cactaceae and Lamiaceae (three types each), Amaranthaceae,
Anacardiaceae,
Brassicaceae,
Convolvulaceae,
Malpighiaceae and Portulacaceae (two types each). Twenty-two
families were represented by only a single pollen type each. Pollen
types that could not be botanically identied were classied as
Unidentied, and these were obtained in 16 samples (Appendix 1,
electronic version, Fig. 1).
Regarding the percentages of the different pollen types in the
samples, 14 types were registered in PP Class (11.9% of the types
identied): Angelonia campestris, Copaifera, Croton, Jatropha,
Microtea, Mimosa lipes, Mimosa misera, Peltogyne pauciora, Piptadenia moniliformis, Prosopis juliora, Rhaphiodon echinus, Spondias
tuberosa, Ziziphus joazeiro and Zornia echinocarpa. SP Class had 18
types (15.3%): A. campestris, Chamaecrista, Cratylia mollis, Croton,
Diodia radula, Eriope, Hypenia salzmanii, M. lipes, M. misera, Pilosocereus tuberculatus, P. moniliformis, Plathymenia reticulata, P.
juliora, R. echinus, Trichilia hirta, Vernonanthura subverticillata, Z.
joazeiro and Z. echinocarpa. IP Class had 37 pollen types (31.45%),
and MP Class had 38 types (32.3%). The majority of the pollen types
occurred in more than one frequency class in the different samples,
although 33 pollen types (28.05%) were only observed at frequencies below 1%, and were classied only as present (Appendix 1,
electronic version).
In terms of the constancy classes, 42 pollen types were
considered rare, 26 types were occasional, 16 types were low
constant. M. misera (Fabaceae) was the only pollen type considered
constant, it is present in 37 samples. The pollen types Angelonia
campestris, Conocliniopsis prasiifolia, Diodia radula, Eriope, Evolvulus
glomeratus, Mimosa lipes, Piptadenia moniliformis, Prosopis juliora,
Rhaphiodon echinus were present in more than 20 samples. These
above mentioned pollen types occurred in various frequency
classes (Appendix 1, electronic version).
Twenty-one species observed owering in the study area in
2004 (Table 1) demonstrated pollen types similar to those recorded
in the pollen collected by A. mellifera, specially between the months
of May and August. Only 15 species demonstrated continuous
owering during the greater part of the year, and many of them had
pollen registers for long periods of time in the pollen-trap samples
collected during the study period (2004e2006).
Comparisons of the pollen records with owering data (even
considering data gathered in different years) are noticeable: a)
Conocliniopsis prasiifolia (DC.) R.M. King & H. Rob. e whose owering period and pollen record are present in continuous period; b)
Pilosocereus tuberculatus (Werderm.) Byles & G.D. Rowley e owering during the entire year, but pollen record are only sporadic
records in the samples of pollen loads; c) Hypenia salzmanii (Benth.)
Harley e owering during the entire year, but pollen records are
concentrated during the months at the end of the rainy season
(JuneeAugust).

Table 1
Comparison between the owering period (>) of 21 species from the Canudos Biological Stations ora in 2004 and the occurrence of their pollen record in samples of bee pollen in 2004 (-), 2005 (:) and 2006 (C).

J. Santos de Novais et al. / Journal of Arid Environments 74 (2010) 1355e1358

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J. Santos de Novais et al. / Journal of Arid Environments 74 (2010) 1355e1358

whose pollen types were observed in the samples analyzed here,

are characteristic of Caatinga regions with sandy soils, as in the CBS.
Other Leguminosae taxa that are commonly found in the Caatinga (Queiroz, 2009) and observed to be important in pollen-trap
collections at the CBS were: Anadenanthera colubrina (Vell.) Brenan,
Poincianella microphylla (Mart. ex G. Don) L.P. Queiroz
[ Caesalpinia microphylla (Mart. ex G.Don)], Cratylia mollis Mart.
ex Benth., Peltogyne pauciora Benth., Piptadenia stipulacea (Benth.)
Ducke, Pityrocarpa moniliformis (Benth.) Luckow & Jobson
[ Piptadenia moniliformis Benth.], Plathymenia reticulata Benth.
and Zornia echinocarpa (Moric.) Benth..
The long list of species identied in pollen studies of bee products
from the semi-arid region reects the dependence of eusocial bees
(A. mellifera and stingless bees) on continuous supplies of nectar and
pollen during the entire year (Santos et al., 2005).
The scarcity of food resources in the Caatinga region during the
dry season (especially between the months of September and
December) is accompanied by a decrease in the richness of pollen
types during that period, and the species that are most important to
these bees during this season (such as Anadenanthera colubrina
(Vell.) Brenan, Commiphora leptophloeos [Mart.] J.B. Gillett and
Croton spp) are seen to be strongly represented. It will be important
to focus future studies on the biology of these plant species due to
their potential usefulness in managed apiculture and meliponiculture activities. The pollination strategies of these species will
need to be investigated in order to evaluate the possible impacts of
the introduction of exotic bee species on the guilds of native
pollinators.
The generalist (polytrophic) pattern of oral resource use by
eusocial bees, such as A. mellifera, that intensively exploit the most
available resources in their foraging area has been demonstrated by
several authors (Cortopassi-Laurino and Ramalho, 1988; Wilms
et al., 1996).
In light of the elevated abundance of Africanized honeybees that
forage on a wide range of plants (many of which are also utilized by
diverse species of native bees) in the Canudos region, pollen studies
evaluating the overlap of trophic niches should be able of detecting
possible competitive pressure exerted by Apis mellifera on native
species. Therefore, these studies assist us to understand ecological
processes related to the maintenance of insect and plant groups
peculiar to xeric regions.
Acknowledgments
We authors gratefully acknowledge Fundao Biodiversitas for
allowing the establishment of this research at CBS, Conselho
Nacional de Desenvolvimento Cientco e Tecnolgico (CNPq) and
Fundao de Amparo Pesquisa do Estado da Bahia (FAPESB) for
grants and nancial support.
Appendix 1. Supplementary material
Pollen map of bee pollen samples (n 62) collected at Canudos
Biological Station, Bahia State, Brazil. P: Predominant pollen. S:

Secondary pollen. Im: Important Minor pollen. m: Minor pollen. p:

present pollen (<1%). CC: constancy classes. R: Rare. O: Occasional. LC: Low Constant. C: Constant.
Supplementary material associated with this article can be
found in the online version, at doi:10.1016/j.jaridenv.2010.05.005.

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