Versatility of the trophic niche of Centris (Paracentris) burgdorfi (Apidae, Centridini)
Tóm tắt
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.
Tài liệu tham khảo
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
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
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
Alves-dos-Santos I, Machado IC, Gaglianone MC (2007) História natural das abelhas coletoras de óleo. Oecol Bras 11(4):544–557
Batagelj V, Mrvar A (1998) Pajek-program for large network analysis. Connections 21(2):47–57
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
Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279
Buchmann SL (1985) Bees use vibration to aid pollen collection from non-poricidal flowers. J Kansas Entomol Soc 58(3):517–525
Buchmann SL (1987) The ecology of oil flowers and their bees. Ann Rev Ecol Syst 18:343–369
Buchmann SL, O’rourke MK (1991) Importance of pollen grain volumes for calculating bee diets. Grana 30(3–4):591–595
Calliari LJ, Klein ADF (1993) Características morfodinâmicas e sedimentológicas das praias oceânicas entre Rio Grande e Chuí, RS. Pesquisas Geocienc 20(1):48–56
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
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
Cocucci A (1991) Pollination biology of Nierembergia (Solanaceae). Plant Syst Evol 174:17–35
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
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
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
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analyzing ecological networks. R News 8:8–11
Erdtman G (1960) The acetolized method. A revised description. Svensk Bot Tidskrift 54:561–564
Gaglianone MC (2001) Nidificação e forrageamento de Centris (Ptilotopus) scopipes Friese (Hymenoptera, Apidae). Rev Bras Zool 18(Supl. 1):107–117
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
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9
Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7(1):69–80
Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford
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
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
Maurizio A, Louveaux J (1965) Pollens de Plantes Mellifères d’Europe. Union des groupements apicoles français, Paris
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
Michener CD (1979) Biogeography of the bees. Ann Missouri Bot Gard 66(3):277–347
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
Montero I, Tormo R (1990) Análisis políınico de mieles de cuatro zonas montanhosas de extremadura. Nacl Asoc Palinol Leng Esp 5:71–78
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
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
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
Pielou EC (1966) An introduction to mathematical ecology. Wiley, New York
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
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
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
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
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
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
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
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
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
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
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
Shannon CEA (1948) Mathematical theory of communication. Bell Syst Technol J 27:379–423
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
Silva JMC, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience 52(3): 225–234
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
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
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
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
Simpson BB (1982) Krameria (Krameriaceae) flowers: orientation and elaiophore morphology. Taxon 31(3):517–528
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
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
Vogel S (1974) Ölblumen und ölsammelnde Bienen. Trop Subtrop Pflanzenwelt 7:285–547
Vogel S (1990) History of the Malpighiaceae in the light of the pollination ecology. Mem NY Bot Gard 55:130–142
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