Abstract
The flora of north-eastern Brazil offers a source of nectariferous–polliniferous species that support many native pollinators. However, few studies have examined the plant–Meliponini interaction, especially from the melissopalynological aspect. We assessed the flora exploited by Tetragonisca angustula in two caatinga (dry vegetation) areas in the Brazilian semi-arid region through pollen analysis of honeys with the goal of answering the following questions: (a) What are the most representative pollens found in the honeys? (b) Do certain pollen types function as regional geographic markers? (c) What are the characteristics of the trophic niche of T. angustula in these areas? The honeys (n = 27) were collected every month from October 2010 to December 2011 in Itaberaba and Ruy Barbosa, diluted in tepid water and 95 % ethanol and subsequently acetolysed. The results revealed 67 pollen types in the honeys, with 25 common to both study areas and most of them belonging to the family Fabaceae (>10 types). The most frequent pollen types were Heteropterys, Mikania, Myrcia, Prosopis juliflora and Solanum for Itaberaba and Heteropterys, Mimosa tenuiflora, P. juliflora, Schinus, Senna macranthera, Solanum and Syagrus coronata for Ruy Barbosa. Anadenanthera colubrina, Poincianella pyramidalis and Ziziphus joazeiro were considered markers for caatinga flora. The amplitude of the trophic niche varied between 0.36 and 2.55, while the evenness ranged from 0.15 to 0.77, characterising the foraging habit of T. angustula as polylectic with a more homogeneous use of the flora in Ruy Barbosa than in Itaberaba.
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References
Aires ERB, Freitas BM (2001) Caracterização palinológica de algumas amostras de mel do Estado do Ceará. Ciên Agron 32(1/2):22–29
Albuquerque UP, Araújo EL, El-Deir ACA, Lima ALA, Souto A, Bezerra BM, Ferraz EMN, Freire EMX, Sampaio EVSB, Las-Casas FMG, Moura GJB, Pereira GA, Melo JG, Ramos MA, Rodal MJN, Schiel N, Lyra-Neves RM, Alves RRN, Azevedo-Júnior SM, Telino Júnior WR, Severi W (2012) Caatinga revisited: ecology and conservation of an important seasonal dry forest. The Scientific World Journal 2012, Article ID 205182. doi:10.1100/2012/205182
Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Cox PA, Dalton V, Feinsinger P, Inouye D, Ingram M, Jones CE, Kennedy K, Nabham GP, Pavlik B, Tepedino V, Torchio P, Walker S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17
Almeida AMM, Carvalho CAL, Abreu RD, Santos FAR, Araújo RCMS, Oliveira PP (2005) Espectro polínico de amostras de mel de Apis mellifera L. provenientes de Nova Soure, Bahia. Rev Agric 80(2):131–147
Alves RMO, Souza BA, Carvalho CAL (2006) Espectro polínico de amostras de mel de Melipona mandacaia Smith, 1863 (Hymenoptera: Apidae). Acta Sci Biol Sci 28(1):33–38
Borges RLB, Lima LCL, Oliveira PP, Silva FHM, Novais JS, Dórea MC, Santos FAR (2006) O pólen no mel do semi-árido brasileiro. In: Santos FAR (ed) Apium plantae. IMSEAR, Recife, PE, pp 103–118
Bryant VM, Jones GD (2001) The r-values of honey: pollen coefficients. Palynology 25:11–28
Cardoso DBOS, Queiroz LP (2008) Floristic composition of seasonally dry tropical forest fragments in Central Bahia, Northeastern Brazil. J Bot Res Inst Tex 2(1):551–573
Carvalho CAL, Nascimento AS, Pereira LL, Machado CS, Clarton L (2006) Fontes nectaríferas e poliníferas utilizadas por Melipona quadrifasciata (Hymenoptera: Apidae) no Recôncavo Baiano. Magistra 18:249–256
Cesário LF, Gaglianone MC (2008) Biologia floral e biologia reprodutiva de Schinus terebinthifolius Raddi (Anacardiaceae) em restinga do Norte Fluminense. Acta Bot Bras 22(3):828–833
Dutra VF, Vieira MF, Garcia FCP, Lima HC (2009) Fenologia reprodutiva, síndromes de polinização e dispersão em espécies de Leguminosae dos campos rupestres do Parque Estadual do Itacolomi, Minas Gerais. Brasil Rodriguésia 60(2):371–387
Erdtman G (1960) The acetolysis method—a revised description. Svensk Bot Tidskr 54(4):561–564
Flores FF, Sánchez AC (2010) Primeros resultados de la caracterización botánica de mieles producidas por Tetragonisca angustula (Apidae, Meliponinae) en Los Naranjos, Salta. Argent Soc Argent Bot 45(1–2):81–91
Freitas BM (1991) Potencial da caatinga para produção de pólen e néctar para a exploração apícola. Dissertation, Federal University of Ceará
Freitas BM, Silva EMS (2006) Potencial apícola da vegetação do Semi-Árido brasileiro. In: Santos FAR (ed) Apium plantae. IMSEAR, Recife, PE, pp 19–32
Freitas BM, Imperatriz-Fonseca VL, Medina LM, Kleinert AMP, Galetto L, Nates-Parra G, Quezada-Euán JJG (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40:332–346. doi:10.1051/apido/2009012
Giannini TC, Acosta AL, Garófalo CA, Saraiva AM, Alves-dos-Santos I, Imperatriz-Fonseca VL (2012) Pollination services at risk: bee habitats will decrease owing to climate change in Brazil. Ecol Model 244:127–131. doi:10.1016/j.ecolmodel.2012.06.035
Giulietti AM, Harley RM, Queiroz LP, Barbosa MRV, Du Bocage Neta AL, Figueiredo MA (2002) Espécies endêmicas da caatinga. In: Sampaio EVSB, Giulietti AM, Virgínio J, Gamarra-Rojas CFL (eds) Vegetação e flora da caatinga. APNE/CNIEB, Recife, PE, pp 103–108
Giulietti AM, Du Bocage Neta AL, Castro AAJF, Gamarra-Rojas CFL, Sampaio EVSB, Virgínio JF, Queiroz LP, Figueiredo MA, Rodal MJN, Barbosa MRV, Harley RM (2004a) Diagnóstico da vegetação nativa do bioma caatinga. In: Silva JMC, Tabarelli M, Fonseca MT, Lins LV (eds) Biodiversidade da caatinga: áreas e ações prioritárias para a conservação. MMA, Brasília, DF, pp 47–90
Giulietti AM, Du Bocage Neta AL, Paula DC, Barbosa DC, Nogueira E, Sampaio EVSB, Silva GC, Machado IC, Virgínio JF, Maia LC, Griz LMS, Queiroz LP, Lima JLS, Silva MA, Figueiredo MA, Rodal MJN, Barradas MM, Barbosa MRV, Harley RM, Chaves SM (2004b) Vegetação: áreas e ações prioritárias para a conservação da caatinga. In: Silva JMC, Tabarelli M, Fonseca MT, Lins LV (eds) Biodiversidade da caatinga: áreas e ações prioritárias para a conservação. MMA, Brasília, DF, pp 113–131
Imperatriz-Fonseca VL, Kleinert-Giovannini A, Cortopassi-Laurino M, Ramalho M (1984) Hábitos de coleta de Tetragonisca angustula angustula Latreille (Apidae, Meliponinae). Bolm Zool Univ S Paulo 8:115–131
Iwama S, Melhem TS (1979) The pollen spectrum of the honey of Tetragonisca angustula angustula Latreille (Apidae, Meliponinae). Apidologie 10(3):275–295. doi:10.1051/apido:19790305
Jones GD, Bryant VM Jr (1996) Melissopalynology. In: Jansonius J, McGregor DC (eds) Palynology: principles and applications, vol 3. AASP Foundation, Dallas, pp 933–938
Jones GD, Bryant VM Jr (2004) The use of ETOH for dilution of honey. Grana 43(3):174–182. doi:10.1080/00173130410019497
Lieux MH (1980) Acetolysis applied to microscopical honey analysis. Grana 19:57–61
Lima LCL (2007) Espécies de Mimosa L. (Leguminosae) do semi-árido nordestino: palinologia, fenologia, biologia floral e potencial apícola. Thesis, Bahia State University at Feira de Santana
Louveaux J, Maurizio A, Vorwohl G (1978) Methods of melissopalynology. Bee World 59(4):139–157
Ludwig JA, Reynolds JF (1988) Statistical ecology: a primer on methods and computing. Wiley, New York
Machado IC, Lopes AV (2003) Recursos florais e sistemas de polinização e sexuais em caatinga. In: Leal IR, Tabarelli M, Silva JMC (eds) Ecologia e conservação da, caatinga edn. Universitária da UFPE, Recife, PE, pp 515–563
Machado ICS, Barros LM, Sampaio EVSB (1997) Phenology of caatinga species at Serra Talhada, PE, Northeastern Brazil. Biotropica 29(1):57–68
Maia-Silva C, Silva CI, Hrncir M, Queiroz RT, Imperatriz-Fonseca VL (2012) Guia de plantas visitadas por abelhas na caatinga. Fundação Brasil Cidadão, Fortaleza, CE
Medeiros SS, Cavalcante AMB, Marin AMP, Tinôco LBM, Salcedo IH, Pinto TF (2012) Sinopse do censo demográfico para o semiárido brasileiro. INSA, Campina Grande, PB
Moar NT (1985) Pollen analysis of New Zealand honey. New Zeal J Agr Res 28:39–70. doi:10.1080/00288233.1985.10426997
Molan P (1998) The limitations of the methods of identifying the floral source of honeys. Bee World 79(2):59–68
Nimer E (1972) Climatologia da região Nordeste do Brasil: introdução à climatologia dinâmica—subsídios à geografia regional do Brasil. R Bras Geogr 34(2):3–51
Novais JS, Lima LCL, Santos FAR (2006) Espectro polínico de méis de Tetragonisca angustula Latreille, 1811 coletados na caatinga de Canudos, Bahia, Brasil. Magistra 18(4):257–264
Obrégon D, Rodríguez A, Chamorro FJ, Nates-Parra G (2013) Botanical origin of pot honey from Tetragonisca angustula Latreille in Colombia. In: Vit P, Pedro SRM, Roubik DW (eds) Pot-honey: a legacy of stingless bees. Springer, Berlin, pp 337–346
Oliveira PP (2009) Análise palinológica de amostras de mel de Apis mellifera L. produzidas no estado da Bahia. Thesis, Bahia State University at Feira de Santana
Oliveira PP, van den Berg C, Santos FAR (2010) Pollen analysis of honeys from Caatinga vegetation of the state of Bahia, Brazil. Grana 49(1):66–75. doi:10.1080/00173130903485122
Pielou EC (1977) Mathematical ecology. Wiley, New York
Prado D (2003) As caatingas da América do Sul. In: Leal IR, Tabarelli M, Silva JMC (eds) Ecologia e conservação da, caatinga edn. Universitária da UFPE, Recife, PE, pp 3–73
Queiroz LP (2006) The Brazilian Caatinga: phytogeographical patterns inferred from distribution data of the Leguminosae. In: Pennington RT, Lewis GP, Ratter JA (eds) Neotropical savannas and dry forests: diversity, biogeography, and conservation. Taylor and Francis, CRC Press, Boca Raton, FL, pp 113–149
Queiroz LP (2008) Leguminosas da caatinga. UEFS, Feira de Santana, BA
Ramalho M, Kleinert-Giovannini A, Imperatriz-Fonseca VL (1990) Important bee plants for stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie 21:469–488. doi:10.1051/apido:19900508
Roubik DW, Moreno PJE (1991) Pollen and spores of Barro Colorado Island. MBG Press, St. Louis, MO
Sampaio EVSB (2002) Uso das plantas da caatinga. In: Sampaio EVSB, Giulietti AM, Virgínio J, Gamarra-Rojas CFL (eds) Vegetação e flora da caatinga. APNE, Recife, PE, pp 49–90
Santos Júnior MC, Santos FAR (2003) Espectro polínico de amostras de méis coletadas na microrregião do Paraguassu, Bahia. Magistra 15(1):79–85
Santos FAR, Oliveira AV, Lima LCL, Barros RFM, Schlindwein CP, Martins CF, Camargo RCR, Freitas BM, Kiill LHP (2005) Apícolas. In: Sampaio EVSB, Pareyn FGC, Figueroa JM, Santos AG Jr (eds) Espécies da flora nordestina com importância econômica potencial. APNE, Recife, PE, pp 15–26
Santos FAR, Oliveira JM, Oliveira PP, Leite KRB, Carneiro CE (2006a) Plantas do semi-árido importantes para as abelhas. In: Santos FAR (ed) Apium plantae. IMSEAR, Recife, PE, pp 61–86
Santos RF, Kiill LHP, Araújo JLP (2006b) Levantamento da flora melífera de interesse apícola no município de Petrolina-PE. Caatinga 19(3):221–227
SEI (2013) Informações geográficas. Sistema de Dados Estatísticos. http://www.sei.ba.gov.br/side/consulta_frame.wsp?tmp.codpai=gr1&tmp.pesquisa=false. Accessed 19 March 2013
Silva FHM (2007) Contribuição à palinologia das caatingas. Thesis, Bahia State University at Feira de Santana
Sodré GS, Marchini LC, Carvalho CAL, Moreti ACCC (2007) Pollen analysis in honey samples from the two main producing regions in the Brazilian northeast. An Acad Bras Ciênc 79(3):381–388
Sosa-Nájera MS, Martínez-Henández E, Lozano-García MS, Cuadriello-Aguiar JI (1994) Nectaropolliniferous sources used by Trigona (Tetragonisca) angustula in Chiapas, southern México. Grana 33(4):225–230. doi:10.1080/00173139409429003
Stehmann JR, Mentz LA, Agra MF, Vignoli-Silva M, Giacomin L (2013) Solanaceae. In: Lista de espécies da flora do Brasil. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB14716. Accessed 29 March 2013
Symon DE (1979) Sex forms in Solanum (Solanaceae) and the role of pollen collecting insects. In: Hawkes JG, Lester RNL, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Academic Press, London, pp 385–397
Zanella FCV, Martins CF (2003) Abelhas da caatinga: biogeografia, ecologia e conservação. In: Leal IR, Tabarelli M, Silva JMC (eds) Ecologia e conservação da, caatinga edn. Universitária da UFPE, Recife, PE, pp 75–134
Zych M, Goldstein J, Roguz K, Stpiczyńska M (2013) The most effective pollinator revisited: pollen dynamics in a spring-flowering herb. Arthropod-Plant Interactions 7:315–322
Acknowledgments
Many thanks to Prof. Carleandro de Souza Dias, M.Sc., for helping us establish contact with bee-keepers and with the Bahia Agricultural Development Company S.A. (Empresa Baiana de Desenvolvimento Agrícola S.A.—EBDA) in Itaberaba, and for providing honey samples from his private bee yard; to the directors of the Mãe Jovina Agricultural Family School (Escola Família Agrícola Mãe Jovina) for granting access to the institution’s bee yard in Ruy Barbosa; to the bee-keepers Alex and Manoel for providing samples; to the intern Bruno Henrique Andrade-Silva for his assistance in monthly collections in the field and in the laboratory; to the regional management and staff of EBDA in Itaberaba for logistical support during field trips; to colleagues from the Laboratory of Plant Micromorphology at the Bahia State University at Feira de Santana (Universidade Estadual de Feira de Santana—UEFS) for help in the laboratory identifying pollen types and for discussions throughout this work; to Leilton Santos Damascena, M.Sc., for help with the map; and to the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq) for partially funding this project and for the grants awarded (processes 575747/2008-0, 143084/2009-7, 303557/2010-9 and 477127/2011-8).
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Novais, J.S., Absy, M.L. & Santos, F.A.R. Pollen grains in honeys produced by Tetragonisca angustula (Latreille, 1811) (Hymenoptera: Apidae) in tropical semi-arid areas of north-eastern Brazil. Arthropod-Plant Interactions 7, 619–632 (2013). https://doi.org/10.1007/s11829-013-9276-x
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DOI: https://doi.org/10.1007/s11829-013-9276-x