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Short Communication

Bee pollen loads and their use in indicating flowering in the Caatinga regionof Brazil

Jaílson Santos de Novais a,*,1, Luciene Cristina Lima e Lima b, Francisco de Assis Ribeiro dos Santos a

a Laboratório de Micromorfologia Vegetal, Programa de Pós-Graduação em Botânica, Universidade Estadual de Feira de Santana, Av. Transnordestina,s/n, Novo Horizonte, 44036-900 Feira de Santana, Bahia, Brazilb Laboratório de Estudos Palinológicos, Departamento de Ciências 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

Article history:Received 25 January 2010Received in revised form6 May 2010Accepted 7 May 2010Available online 2 June 2010

Keywords:Apis melliferaBeekeepingMelissopalynologyPhenologyPollen spectrumSemi-arid

a b s t r a c t

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-trapsbetween March/2004 and February/2006 were examined. The pollen loads were acetolyzed and thepollen types identified and counted by sampling using an optical microscope. Thirty-six plant familieswere found to contribute to the composition of the pollen spectrum of the samples, with 85 differentpollen types. Fabaceae was the most represented family (21 pollen types), and Mimosa filipes was thesingle most frequently observed pollen type (37 samples). The predominant pollen class included 14pollen 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 apiculturalpotential, such as Croton spp., Spondias tuberosa Arruda and Ziziphus joazeiro Mart., were well repre-sented in the pollen spectrum. The pollen map was found to be useful for indicating the floweringperiods of certain Caatinga species if long and continuous observations were made.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Pollen is a vital product for bees, principally due to its criticalrole in the diet of their larvae (Wiese, 1985). Plants contributegreatly to the sustenance of these insects, and they are in turn ofnotable importance in the pollination and reproduction of manyplant groups (Simpson and Neff, 1983).

Apis mellifera L. is a very successful bee species due to itscapacity to adapt to diverse environments and to out-competemany species of native bees. Since the 1950s, honeybees have beenintroduced into (and raised in) the entire Brazil, including the drynortheast region (Santos, 2006).

Studies of the pollen loads of A. mellifera have contributed toa systematized characterization of the apicultural flora in manycountries, and have been especially useful in providing information

to beekeepers (Biesmeijer et al., 1992; Webby, 2004; Andrada andTellería, 2005; Dimou and Thrasyvoulou, 2007). Studies of thistype are still few in Brazil and are still far from being able to furnishdetailed information about the diversity and potential of the nativeapicultural flora (Carvalho et al., 1999; Marchini et al., 2000; Novaiset al., 2009).

Activities such as apiculture and meliponiculture have animportant role in the subsistence economies of many localities inthe semi-arid region of Brazil, and these activities contribute tosustainable regional development by using resources naturallysupplied by the flora and fauna characteristic of the Caatingabiome. As such, melissopalynological studies can offer valuableinformation about apiculture and meliponiculture products(mainly valuable in terms of exportation markets) as they canindicate botanical and geographical origin of the products (Santos,2006; Oliveira et al., 2010).

This study presents a pollen map of the pollen loads transportedby Africanized honeybees in an area of Caatinga vegetation innortheastern Brazil. Additionally, as the pollen spectrum ofapiculture products reflects the flora available to the bees, weinvestigated the usefulness of this pollen data in providing infor-mation about the flowering of plants utilized by these insects in thestudy area.

* Corresponding author. Tel.: þ55 75 3224 8238; fax: þ55 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 Formação Interdisciplinar, Universidade Federal do

Oeste do Pará, Av. Marechal Rondon, s/n, Caranazal, 68060-070 Santarém, Pará,Brazil.

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0140-1963/$ e see front matter � 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.jaridenv.2010.05.005

Journal of Arid Environments 74 (2010) 1355e1358

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2. Material and methods

2.1. Study area

The Canudos Biological Station (CBS) is managed by the Fun-dação Biodiversitas, and it is located in the municipality of Canudosin the northeastern micro-region of Bahia State, Brazil (09�540S,39�070W, altitude: 400 m). The CBS experiences average annualtemperatures of 24.15 �C, with November through March being thewarmest season of the year and the period of greatest rainfall,although annual precipitation usually amounts to less than400 mm (SEI, 1998).

The vegetation in the CBS is predominantly composed ofshrubby hyperxerophytic Caatinga whose floristic composition hasa 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 inthe study area. The pollen-traps were placed at the entrances of thehives by a 24-h period, starting at 18.00 h. The samples were pro-cessed in the Plant Micromorphology Laboratory (LAMIV) of theUniversidade Estadual de Feira de Santana (UEFS), Feira de Santana,Bahia State, Brazil.

The samples were prepared by dehydrating the pollen loads ina drying oven at 40 �C until attaining a constant weight and weresubsequently processed using the methodology of Alvarado andDelgado (1985), with modifications described by Novais et al.

(2009). The pollen sediments were acetolyzed according to theprocedures described by Erdtman (1960).

Each acetolyzed sample was mounted in glycerin jelly on four ormore slides; one preparation was mounted in glycerin jelly stainedwith safranin. All of the slides were subsequently deposited in theLAMIV/UEFS pollen library.

After identifying the pollen types present on the slides, at least1200 pollen grains were counted using sampling methods toestablish 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 typein the samples, we adopted the following constancy classes: VeryConstant (present in >75% of the samples), Constant (>50e�75%),Low Constant (>25e�50%), Occasional (�e�25%) and Rare (<5%)(Novais et al., 2009).

Pollen library samples at LAMIV, as well as palynological refer-ence catalogs were used to determine the botanical affinity of thepollen types.

Information concerning the flowering of some of the species atthe CBS was obtained during monthly surveys in 2004 by Silva(2007) and is presented here and compared to the pollen datagathered from the hives.

3. Results

A total of 85 different pollen types were identified 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: Caesalpiniamicrophylla, Cp: Conocliniopsis prasiifolia, Dr: Diodia radula, Jr: Jatropha ribifolia, Le: Lippia elegans, Mb: Mitracarpus baturitensis, Mm: Mimosa misera, Pj: Prosopis juliflora, Pr: Pla-thymenia reticulata, Re: Rhaphiodon echinus, Tm: Turnera melochioides, Vs: Vernonanthura subverticillata and, Z: Zornia. Scale bars ¼ 30 mm.

J. Santos de Novais et al. / Journal of Arid Environments 74 (2010) 1355e13581356

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Euphorbiaceae, Malvaceae s.l. and Rubiaceae (five types each), Poa-ceae (four), Cactaceae and Lamiaceae (three types each), Amar-anthaceae, Anacardiaceae, Brassicaceae, Convolvulaceae,Malpighiaceae and Portulacaceae (two types each). Twenty-twofamilies were represented by only a single pollen type each. Pollentypes that could not be botanically identified were classified as“Unidentified”, and these were obtained in 16 samples (Appendix 1,electronic version, Fig. 1).

Regarding the percentages of the different pollen types in thesamples, 14 types were registered in PP Class (11.9% of the typesidentified): Angelonia campestris, Copaifera, Croton, Jatropha,Microtea, Mimosa filipes, Mimosa misera, Peltogyne pauciflora, Pip-tadenia moniliformis, Prosopis juliflora, Rhaphiodon echinus, Spondiastuberosa, Ziziphus joazeiro and Zornia echinocarpa. SP Class had 18types (15.3%): A. campestris, Chamaecrista, Cratylia mollis, Croton,Diodia radula, Eriope, Hypenia salzmanii, M. filipes, M. misera, Pilo-socereus tuberculatus, P. moniliformis, Plathymenia reticulata, P.juliflora, 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 typesoccurred in more than one frequency class in the different samples,although 33 pollen types (28.05%) were only observed at frequen-cies below 1%, and were classified only as “present” (Appendix 1,electronic version).

In terms of the constancy classes, 42 pollen types wereconsidered rare, 26 types were occasional, 16 types were lowconstant.M. misera (Fabaceae) was the only pollen type consideredconstant, it is present in 37 samples. The pollen types Angeloniacampestris, Conocliniopsis prasiifolia, Diodia radula, Eriope, Evolvulusglomeratus, Mimosa filipes, Piptadenia moniliformis, Prosopis juliflora,Rhaphiodon echinus were present in more than 20 samples. Theseabove mentioned pollen types occurred in various frequencyclasses (Appendix 1, electronic version).

Twenty-one species observed flowering in the study area in2004 (Table 1) demonstrated pollen types similar to those recordedin the pollen collected by A. mellifera, specially between themonthsof May and August. Only 15 species demonstrated continuousflowering during the greater part of the year, andmany of them hadpollen registers for long periods of time in the pollen-trap samplescollected during the study period (2004e2006).

Comparisons of the pollen records with flowering data (evenconsidering data gathered in different years) are noticeable: a)Conocliniopsis prasiifolia (DC.) R.M. King & H. Rob. e whose flow-ering period and pollen record are present in continuous period; b)Pilosocereus tuberculatus (Werderm.) Byles & G.D. Rowley e flow-ering during the entire year, but pollen record are only sporadicrecords in the samples of pollen loads; c)Hypenia salzmanii (Benth.)Harley e flowering during the entire year, but pollen records areconcentrated during the months at the end of the rainy season(JuneeAugust).

4. Discussion

Pollen types of the family Fabaceae have occurred veryfrequently in pollen analyses undertaken in semi-arid regions inBrazil and demonstrated the importance of this plant group toAfricanized honeybees (Sodré et al., 2007; Novais et al., 2009),eusocial native bees (Novais et al., 2006), and solitary species(Dórea et al., 2009).

Among the Fabaceae, the genus Mimosa is very important forproviding floral resources to bees. According to biogeographicaldata of Queiroz (2009), the genusMimosa is well represented in dryregions and has the greatest diversity among the different Fabaceaegenera found in Caatinga areas. Mimosa arenosa (Willd.) Poir. var.arenosa, M. filipes Mart., M. lewisii Barneby, and M. misera Benth., Ta

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J. Santos de Novais et al. / Journal of Arid Environments 74 (2010) 1355e1358 1357

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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 Caa-tinga (Queiroz, 2009) and observed to be important in pollen-trapcollections at the CBS were: Anadenanthera colubrina (Vell.) Brenan,Poincianella microphylla (Mart. ex G. Don) L.P. Queiroz[ ¼ Caesalpinia microphylla (Mart. ex G.Don)], Cratylia mollis Mart.ex Benth., Peltogyne pauciflora Benth., Piptadenia stipulacea (Benth.)Ducke, Pityrocarpa moniliformis (Benth.) Luckow & Jobson[ ¼ Piptadenia moniliformis Benth.], Plathymenia reticulata Benth.and Zornia echinocarpa (Moric.) Benth..

The long list of species identified inpollen studies of bee productsfrom the semi-arid region reflects the dependence of eusocial bees(A.mellifera and stingless bees) on continuous supplies of nectar andpollen during the entire year (Santos et al., 2005).

The scarcity of food resources in the Caatinga region during thedry season (especially between the months of September andDecember) is accompanied by a decrease in the richness of pollentypes during that period, and the species that aremost important tothese bees during this season (such as Anadenanthera colubrina(Vell.) Brenan, Commiphora leptophloeos [Mart.] J.B. Gillett andCroton spp) are seen to be strongly represented. It will be importantto focus future studies on the biology of these plant species due totheir potential usefulness in managed apiculture and meliponi-culture activities. The pollination strategies of these species willneed to be investigated in order to evaluate the possible impacts ofthe introduction of exotic bee species on the guilds of nativepollinators.

The generalist (polytrophic) pattern of floral resource use byeusocial bees, such as A. mellifera, that intensively exploit the mostavailable resources in their foraging area has been demonstrated byseveral authors (Cortopassi-Laurino and Ramalho, 1988; Wilmset al., 1996).

In light of the elevated abundance of Africanized honeybees thatforage on awide range of plants (many of which are also utilized bydiverse species of native bees) in the Canudos region, pollen studiesevaluating the overlap of trophic niches should be able of detectingpossible competitive pressure exerted by Apis mellifera on nativespecies. Therefore, these studies assist us to understand ecologicalprocesses related to the maintenance of insect and plant groupspeculiar to xeric regions.

Acknowledgments

We authors gratefully acknowledge Fundação Biodiversitas forallowing the establishment of this research at CBS, ConselhoNacional de Desenvolvimento Científico e Tecnológico (CNPq) andFundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) forgrants and financial support.

Appendix 1. Supplementary material

Pollen map of bee pollen samples (n ¼ 62) collected at CanudosBiological 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: Occa-sional. LC: Low Constant. C: Constant.

Supplementary material associated with this article can befound in the online version, at doi:10.1016/j.jaridenv.2010.05.005.

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