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Versatility of the trophic niche of Centris (Paracentris) burgdorfi (Apidae, Centridini)

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Abstract

Centris species collect floral oil and use this resource in larval food and for waterproofing their cells. We investigated the trophic niche of three distinct populations of Centris burgdorfi, a widely distributed bee in Brazil, by using pollen collected from female bees. Our goal was to determine whether there is versatility regarding sources of oil, nectar, and pollen in different regions of Brazil. By using the pollen, we also determined whether the source of oil used corresponded to the collection apparatus of the females. In total, we sampled 150 C. burgdorfi females and their associated pollen in three distinct habitat types across Brazil. We prepared pollen by acetolysis and performed quantitative analysis on 400 grains per bee. We identified 41 plant species belonging to 18 families that were used by C. burgdorfi. Although none of the plant species used by C. burgdorfi were shared among areas, the Chamaecrista genus was present in the diet at all three sites. The probable oil source came from plants of the genus Krameria, a genus with epithelial elaiophores. In regions where the Krameriaceae family was not present (e.g., southern Brazil), bees used Angelonia integerrima, a plant with trichomate elaiophores, demonstrating that C. burgdorfis exhibited versatility in its dietary breadth among the studied regions. C. burgdorfi proved to be locally specialized in oil floral source and selectivity in pollen sources, but a generalist when evaluated the wide geographic distribution.

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References

  • Aguiar CML (2003) Flower visits of Centris bees (Hymenoptera: Apidae) in an area of caatinga (Bahia, Brazil). Stud Neotrop Fauna Environ 38(1):41–45

    Article  Google Scholar 

  • Aleixo KP, Faria LB, Garófalo CA, Fonseca VLI, Silva CI (2013) Pollen collected and foraging activities of Frieseomelitta varia (Lepeletier) (Hymenoptera: Apidae) in an urban landscape. Sociobiology 60(3):266–276

    Article  Google Scholar 

  • Alvares CA, Stape JL, Sentelhas PC, de Moraes G, Leonardo J, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22(6):711–728

    Article  Google Scholar 

  • Alves-dos-Santos I, Machado IC, Gaglianone MC (2007) História natural das abelhas coletoras de óleo. Oecol Bras 11(4):544–557

    Article  Google Scholar 

  • Batagelj V, Mrvar A (1998) Pajek-program for large network analysis. Connections 21(2):47–57

    Google Scholar 

  • Bezerra ES, Lopes AV, Machado IC (2009) Biologia reprodutiva de Byrsonima gardnerana A. Juss. (Malpighiaceae) e interações com abelhas Centris (Centridini) no Nordeste do Brasil. Rev Bras Bot 32(1):95–108

    Article  Google Scholar 

  • Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279

    Article  Google Scholar 

  • Buchmann SL (1985) Bees use vibration to aid pollen collection from non-poricidal flowers. J Kansas Entomol Soc 58(3):517–525

    Google Scholar 

  • Buchmann SL (1987) The ecology of oil flowers and their bees. Ann Rev Ecol Syst 18:343–369

    Article  Google Scholar 

  • Buchmann SL, O’rourke MK (1991) Importance of pollen grain volumes for calculating bee diets. Grana 30(3–4):591–595

    Article  Google Scholar 

  • Calliari LJ, Klein ADF (1993) Características morfodinâmicas e sedimentológicas das praias oceânicas entre Rio Grande e Chuí, RS. Pesquisas Geocienc 20(1):48–56

    Google Scholar 

  • Cane JH, Sipes S (2006) Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions, from specialization to generalization. University of Chicago Press, Chicago, pp 99–122

    Google Scholar 

  • Carneiro LT, Aguiar AJC, Martins CF, Machado IC, Alves-dos-Santos I (2015) Krameria tomentosa oil flowers and their pollinators: bees specialized on trichome elaiophores exploit its epithelial oil glands. Flora 215:1–8

    Article  Google Scholar 

  • Cocucci A (1991) Pollination biology of Nierembergia (Solanaceae). Plant Syst Evol 174:17–35

    Article  Google Scholar 

  • Dórea MC (2010b) Residual pollen in nests of Centris analis (Hymenopera, Apidae, Centridini) in an area of Caatinga vegetation from Brazil. Oecol Aust 14(1):232–237

    Article  Google Scholar 

  • Dórea MC, Santos FAR, Lima LCL, Figueroa LER (2009) Análise polínica do resíduo pós-emergência de ninhos de Centris tarsata Smith (Hymenoptera: Apidae, Centridini). Neotrop Entomol 38(2):197–202

    Article  Google Scholar 

  • Dórea MC, Aguiar CM, Figueroa LER, Lima LCL, Santos FAR (2010a) Pollen residues in nests of Centris tarsata Smith (Hymenoptera, Apidae, Centridini) in a tropical semiarid area in NE Brazil. Apidologie 41(5):557–567

    Article  Google Scholar 

  • Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analyzing ecological networks. R News 8:8–11

    Google Scholar 

  • Erdtman G (1960) The acetolized method. A revised description. Svensk Bot Tidskrift 54:561–564

    Google Scholar 

  • Gaglianone MC (2001) Nidificação e forrageamento de Centris (Ptilotopus) scopipes Friese (Hymenoptera, Apidae). Rev Bras Zool 18(Supl. 1):107–117

    Article  Google Scholar 

  • Gonçalves RB, Melo GAR (2005) A comunidade de abelhas (Hymenoptera, Apidae s.l) em uma área restrita de campo natural no Parque Estadual de Vila Velha, Paraná: diversidade, fenologia e fontes florais de alimento. Rev Bras Entomol 49(4):557–571

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7(1):69–80

    Article  Google Scholar 

  • Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford

    Google Scholar 

  • Martins AC, Melo GAR (2015) The New World oil-collecting bees Centris and Epicharis (Hymenoptera, Apidae): molecular phylogeny and biogeographic history. Zool Scripta 1–12

  • Martins AC, Aguiar AJC, Alves-dos-Santos I (2013) Interaction between oil-collecting bees and seven species of Plantaginaceae. Flora 208(7):401–411

    Article  Google Scholar 

  • Martins AC, Melo GAR, Renner SS (2014) The corbiculate bees arose from New World oil-collecting bees: implications for the origin of pollen baskets. Mol Phylogenet Evol 80:88–94

    Article  PubMed  Google Scholar 

  • Maurizio A, Louveaux J (1965) Pollens de Plantes Mellifères d’Europe. Union des groupements apicoles français, Paris

    Google Scholar 

  • Mello MAR, Bezerra ELS, Machado IC (2013) Functional roles of centridini oil bees and malpighiaceae oil flowers in biome-wide pollination networks. Biotropica 45(1):45–53

    Article  Google Scholar 

  • Michener CD (1979) Biogeography of the bees. Ann Missouri Bot Gard 66(3):277–347

    Article  Google Scholar 

  • Minckley RL, Roulston TH (2006) Incidental mutualisms and pollen specialization among bees. In: Waser NM, Ollerton J (eds) Plant-pollination interactions: from specialization to generalization. University Chicago Press, Chicago, pp 69–98

    Google Scholar 

  • Montero I, Tormo R (1990) Análisis políınico de mieles de cuatro zonas montanhosas de extremadura. Nacl Asoc Palinol Leng Esp 5:71–78

    Google Scholar 

  • Neff JL, Simpson BB (1981) Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematics. J Kansas Entomol Soc 54(1):95–123

    Google Scholar 

  • Oliveira R, Schlindwein C (2009) Searching for a manageable pollinator for acerola orchards: the solitary oil-collecting bee Centris analis (Hymenoptera: Apidae: Centridini). J Econ Entomol 102(1):265–273

    Article  PubMed  Google Scholar 

  • Oliveira GA, Aguiar CML, Silva M, Gimenes M (2013) Centris aenea (Hymenoptera, Apidae): a ground-nesting bee with high pollination efficiency in Malpighia emarginata DC (Malpighiaceae). Sociobiology 60(3):317–322

    Article  Google Scholar 

  • Pielou EC (1966) An introduction to mathematical ecology. Wiley, New York

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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(5):469–488

    Article  Google Scholar 

  • Renner SS, Schaefer H (2010) The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philos Trans R Soc B 365(1539):423–435

    Article  CAS  Google Scholar 

  • Roberts RB, Vallespir SR (1978) Specialization of hairs bearing pollen and oil on the legs of bees (Apoidea: Hymenoptera). Ann Entomol Soc Am 71:619–627

    Article  Google Scholar 

  • Roig-Alsina A (2000) Claves para las especies argentinas de Centris (Hymenoptera, Apidae), con descripción de nuevas especies y notas sobre distribución. Rev Mus Argent Cienc Nat 2(2):171–193

    Article  Google Scholar 

  • Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17(3):388–400

    Article  PubMed  Google Scholar 

  • Roulston TH, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecol Monogr 70(4):617–643

    Google Scholar 

  • Santos RM, Aguiar CM, Dórea MC, Almeida GF, Santos FAR, Augusto SC (2013) The larval provisions of the crop pollinator Centris analis: pollen spectrum and trophic niche breadth in an agroecosystem. Apidologie 44(6):630–641

    Article  Google Scholar 

  • Schlindwein C (1998) Frequent oligolecty characterizing a diverse bee–plant community in a xerophytic bushland of subtropical Brazil. Stud Neotrop Fauna Environ 33:46–59

    Article  Google Scholar 

  • Schlindwein C (2000) A importância de abelhas especializadas na polinização de plantas nativas e conservação do meio ambiente. In: IV Encontro Sobre Abelhas Encontro Sobre Abelhas. Ribeirão Preto, Anais, pp 131–141

    Google Scholar 

  • Schlindwein C (2004a) Abelhas solitárias e flores: especialistas são polinizadores efetivos? In: Livro de Trabalhos Completos. 55° Congresso Nacional de Botânica, 26° Encontro Regional de Botânicos de MG, BA, ES, Viçosa, MG, 2004, Sociedade Botânica do Brasil. pp 1–8

  • Schlindwein C (2004b) Are oligolectic bees always the most effective pollinators. In: Solitary bees. Conservation, rearing and management for pollination. Imprensa Universitária, Fortaleza, pp 231–240

    Google Scholar 

  • Shannon CEA (1948) Mathematical theory of communication. Bell Syst Technol J 27:379–423

    Article  Google Scholar 

  • Sigrist MR, Sazima M (2004) Pollination and reproductive biology of twelve species of Neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Ann Bot 94:33–41

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva JMC, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52(3): 225–234

    Article  Google Scholar 

  • Silva CI, Imperatriz-Fonseca VL, Groppo M, Bauermann SG, Saraiva AA et al (2014) Catálogo Polínico das Plantas Usadas por Abelhas no Campus da USP de Ribeirão Preto. Holos, Ribeirão Preto

    Google Scholar 

  • Silva CI, Nascimento MM, Alves-dos-Santos IA, Garófalo CA (2016) High prevalence of Miconia chamissois (Melastomataceae) pollen in brood cell provisions of the orchid bee Euglossa townsendi in São Paulo State, Brazil. Apidologie 47(6):855–866

    Article  Google Scholar 

  • Silva CI, Hirotsu CM, Pacheco-Filho AJS, Queiroz EP, Garófalo CA (2017) Is the maximum reproductive rate of Centris analis (Hymenoptera, Apidae, Centridini) associated with floral resource availability? Arthropod Plant Interact 11:1–14

    Article  CAS  Google Scholar 

  • Silveira FA (1991) Influence of pollen grain volume on the estimation of the relative importance of its source to bees. Apidologie 22(5):495–502

    Article  Google Scholar 

  • Simpson BB (1982) Krameria (Krameriaceae) flowers: orientation and elaiophore morphology. Taxon 31(3):517–528

    Article  Google Scholar 

  • Simpson BB, Neff JL, Dieringer G (1990) The production of floral oils by Monttea (Scrophulariaceae) and the function of tarsal pads in Centris bees. Plant Syst Evol 173:209–222

    Article  Google Scholar 

  • Taniguchi M (2010) Morfologia das estruturas envolvidas na coleta e transporte de óleo floral por fêmeas do gênero Centris (Hymenoptera, Apidae). Dissertation, Universidade de São Paulo

  • Tasei JN, Picart M (1973) Le comportement de nidification chez Osmia (Osmia) cornuta. Megachilidae). Apidologie 4(3):195–225

    Article  Google Scholar 

  • Vogel S (1974) Ölblumen und ölsammelnde Bienen. Trop Subtrop Pflanzenwelt 7:285–547

    Google Scholar 

  • Vogel S (1990) History of the Malpighiaceae in the light of the pollination ecology. Mem NY Bot Gard 55:130–142

    Google Scholar 

  • Wcislo WT, Cane JH (1996) Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annu Rev Entomol 41(1):257–286

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to Paulo Roberto de Castro for help and all the support in the field work, and Ana Carolina Oliveira da Silva and Elisa Pereira Queiroz for taking all the measurements of the pollen grains. We also thank to Astrid Kleinert, Celso Feitosa Martins, Clemens Peter Schlindwein, Felipe Vivallo, Liz Nichols, Maria Cristina Gaglianone and the three anonymous reviewers for comments and suggestions on the manuscript. The research was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Rede de Catálogos Polínicos online (RCPol).

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Correspondence to William O. Sabino.

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Sabino, W.O., Alves-dos-Santos, I. & da Silva, C.I. Versatility of the trophic niche of Centris (Paracentris) burgdorfi (Apidae, Centridini). Arthropod-Plant Interactions 13, 227–237 (2019). https://doi.org/10.1007/s11829-018-9654-5

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