High diversity of bees detected in guarana crop and natural habitat due to the use of combined sampling methods
DOI:
https://doi.org/10.12741/ebrasilis.v14.e975Keywords:
Amazon, Apoidea, Malaise, diversity, hand-netting, pan-trapAbstract
Bees are the main pollinators of native and agricultural plants. Identifying and knowing these insects responsible for the environmental service of pollination is essential for the maintenance and management of pollination in agricultural systems, especially in a high diversity biome as the Amazon rainforest. Some crops in this region are dependent of benefited by wild pollinators, especially native plants like guarana. To address methodological aspects of monitoring bee diversity, samplings were carried out in an agricultural environment (guarana crop, Paullinia cupana) surrounded by Amazon natural habitat at Manaus, Amazonas State. We used three combined methods (two passive traps: Malaise and yellow pan-traps, and one active: hand nets) in different periods, with the same number of samplings (12 each). In total, 4,143 native bees belonging to 171 species were sampled; 117 species (1,926 individuals) were collected with Malaise trap, 15 (91 individuals) with pan-traps, and 114 (2,126 individuals) through active sampling. Only seven species were common to all methods, 60 species on two methods and 104 species were unique to one sampling method (50 with Malaise, two with pan-traps, and 52 with hand nets). We reinforce the need for complementary sampling to known bee diversity as the best strategy here was the joint use of active samples and Malaise traps. Recently the concern with Amazon preservation has aroused worldwide interest, a fact that shreds of evidence the need for studies of biodiversity and taxonomy in several areas, since very little is known of this vast region.
References
Absy, ML, AR Rech & MG Ferreira MG, 2018. Pollen Collected by Stingless Bees: A Contribution to Understanding Amazonian Biodiversity, pp 29-46. In: Vit P, SRM Pedro & DW Roubik (Eds.). Pot-Pollen in Stingless Bee Melittology. Springer International Publishing. DOI: https://doi.org/10.1007/978-3-319-61839-5_3
Antonio, IC, 2017. Estação Agroclimatológica da Embrapa Amazônia Ocidental na Rodovia AM-010, Km 29-Manaus. Amazônia Ocidental: EMBRAPA (Boletim agrometeorológico, 60).
Ascher, JS & J Pickering, 2018. Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). Available in: <https://www.discoverlife.org/mp/20q?guide=Apoidea_species>. [Access: 01.vii.2019].
Bezerra, LA, AJ Campbell, TF Brito, C Menezes & M Maués, 2020. Pollen Loads of Flower Visitors to Açaí Palm (Euterpe oleracea) and Implications for Management of Pollination Services. Neotropical Entomology, 49: 482-490. DOI: https://doi.org/10.1007/s13744-020-00790-x
Biesmeijer, JC, SPM Roberts, M Reemer, R Ohlemüller, M Edwards, T Peeters, AP Schaffers, SG Potts, R Kleukers, CD Thomas, J Setteleand & WE Kunin, 2006. Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands. Science, 313: 351-354. DOI: https://doi.org/10.1126/science.1127863
Borges, RC, K Padovani, VL Imperatriz-Fonseca & TC Giannini, 2020. A dataset of multi-functional ecological traits of Brazilian bees. Scientific Data, 7: 120. DOI: https://doi.org/10.1038/s41597-020-0461-3
Campbell, AJ, LG Carvalheiro, MM Maués, R Jaffé, TC Giannini, MAB Freitas, BT Coelho & C Menezes, 2018. Anthropogenic disturbance of tropical forests threatens pollination services to açaí palm in the Amazon river delta. J-ournal of Applied Ecology, 55: 1725-1736. DOI: https://doi.org/10.1111/1365-2664.13086
Camargo, JMF, 1970. Ninhos e biologia de algumas espécies de Meliponideos (Hymenoptera: Apidae) da região de Pôrto Velho, Território de Rondônia, Brasil. Revista de Biología Tropical, 16: 207-239.
Cardoso, P, F Rigal & JC Carvalho, 2015. BAT - Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods in Ecology and Evolution, 6: 232-326. DOI: https://doi.org/10.1111/2041-210X.12310
Corlett, RT, RB Primack, V Devictor, B Maas, VR Goswami, AE Bates, LP Koh, TJ Regan, R Loyola, RJ Pakeman, GS Cumming, A Pidgeon, D Johns & R Roth, 2020. Impacts of the coronavirus pandemic on biodiversity conservation. Biological Conservation, 246: 108571. DOI: https://doi.org/10.1016/j.biocon.2020.108571
Ducke, A, 1906. Neue Beobachtungen über die Bienen der Amazonasländer. Zeitschrift für wissenschaftliche Insektenbiologie, 2: 51-60.
Ellwanger, JH, B Kulmann-Leal, VL Kaminski, JM Valverde-Villegas, ABG da Veiga, FR Spilki, PM Fearnside, L Caesar, LL Giatti, GL Wallau, SEM Almeida, MR Borba, VP da Hora & JAB Chies, 2020. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. Anais da Academia Brasileira de Ciências, 92: e20191375. DOI: https://doi.org/10.1590/0001-3765202020191375
Escobar, JR, MPF Corrêa & FP Aguilera, 1984. Estruturas florais, floração e técnicas para a polinização controlada do guaranazeiro. Pesquisa Agropecuária Brasileira, 19: 615-622.
Foley, JA, GP Asner, MH Costa, MT Coe, R de Fries, HK Gibbs, EA Howard, S Olson, J Patz, N Ramankutty & P Snyder, 2007. Amazonia revealed: forest degradation and loss of ecosystem goods and services in the Amazon Basin. Frontiers in Ecology and the Environment, 5: 25-32. DOI: https://doi.org/10.1890/1540-9295(2007)5[25:ARFDAL]2.0.CO;2
Giannini, TC, S Boff, GD Cordeiro, EA Cartolano, AK Veiga, VL Imperatriz-Fonseca & AM Saraiva, 2015. Crop pollinators in Brazil: a review of reported interactions. Apidologie, 46: 209-223. DOI: https://doi.org/10.1007/s13592-014-0316-z
Giannini, TC, WF Costa, RC Borges, C Cabral, L Miranda, CPW Costa, AM Saraiva & VL Imperatriz-Fonseca, 2020. Climate change in the Eastern Amazon: crop-pollinator and occurrence-restricted bees are potentially more affected. Regional Environmental Change, 20: 9. DOI: https://doi.org/10.1007/s10113-020-01611-y
Gonçalves, RB & CRF Brandão, 2008. Diversidade de abelhas (Hymenoptera, Apidae) ao longo de um gradiente latitudinal na Mata Atlântica. Biota Neotropica, 8: 51-61. DOI: https://doi.org/10.1590/S1676-06032008000400004
Hammer, Ø, DAT Harper & PD Ryan, 2001. PAST: Paleontological statistics software package for education and data analysis. Paleontologia eletronica, 4: 9. Available in: <https://palaeo-electronica.org/2001_1/past/past.pdf>
Hipólito, J, J Coutinho, T Mahlmann, TBR Santana & WE Magnusson, 2021. Legislation and pollination: Recommendations for policymakers and scientists. Perspectives in Ecology and Conservation, 19: 1-9. DOI: https://doi.org/10.1016/j.pecon.2021.01.003
Hortal, J, F de Bello, JAF Diniz-Filho, TM Lewinsohn, JM Lobo & RJ Ladle, 2015. Seven Shortfalls that Beset Large-Scale Knowledge of Biodiversity. Annual Review of Ecology, Evolution and Systematics, 46: 523-549. DOI: https://doi.org/10.1146/annurev-ecolsys-112414-054400
IBGE, 2021. Instituto Brasileiro de Geografia e Estatística. Projeção da população brasileira e das unidades da federação. Available on <http://tabnet.datasus.gov.br/cgi/deftohtm.exe?ibge/cnv/projpopuf.def>. [Access: 01.vi.2020]
Klein, A-M, BE Vaissière, JH Cane, I Steffan-Dewenter, SA Cunningham, C Kremem & T Tscharnke, 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274: 303-313. DOI: https://doi.org/10.1098/rspb.2006.3721
Köppen, W, 1936. Das geographische system der klimate. Hundbuch der Klimatologie, 1st Ed. Berlin, Gebrüder Borntraeger.
Kress, WJ, WR Heyer, P Acevedo, J. Coddington, D Cole, TL Erwin, BJ Meggers, M Pogue, RW Thorington, R P Vari, MJ Weitzman & SH Weitzman, 1998. Amazonian biodiversity: assessing conservation priorities with taxonomic data. Biodiversity and Conservation, 7: 1577-1587. DOI: https://doi.org/10.1023/A:1008889803319
Krug, C & I Alves-dos-Santos, 2008. O uso de diferentes métodos para amostragem da fauna de abelhas (Hymenoptera: Apoidea), um estudo em floresta ombrófila mista em Santa Catarina. Neotropical Entomology, 37: 265-278. DOI: https://doi.org/10.1590/S1519-566X2008000300005
Krug, C, GD Cordeiro, I Schäffler, CI Silva, R Oliveira, C Schlindwein, S Dötterl & I Alves-dos-Santos, 2018. Nocturnal Bee Pollinators Are Attracted to Guarana Flowers by Their Scents. Frontier in Plant Science, 9: 1072. DOI: https://doi.org/10.3389/fpls.2018.01072
Krug, C, MVB Garcia & FB Gomes, 2015. A scientific note on new insights in the pollination of guarana (Paullinia cupana var. sorbilis). Apidologie, 46: 164-166. DOI: https://doi.org/10.1007/s13592-014-0304-3
Lewis, CN & JB Whitfield, 1999. Braconid Wasp (Hymenoptera: Braconidae) Diversity in Forest Plots Under Different Silvicultural Methods. Environmental Entomology, 28: 986-997. DOI: https://doi.org/10.1093/ee/28.6.986
Mahlmann, T, J Hipólito, M Montefusco & C Krug, 2020. First record of the neotropical subgenus Hylaeus (Gongyloprosopis) Snelling, 1982, for Brazil (Hymenoptera: Colletidae). Entomological Communications, 2: ec02012. DOI: https://doi.org/10.37486/2675-1305.ec02012
Maués, MM, C Krug, LHO Wadt, PM Drumond, MC Cavalcante & ACS Santos, 2015. A castanheira-do-brasil: avanços no conhecimento das práticas amigáveis à polinização. 1 Ed. Rio de Janeiro, Fundo Brasileiro para a Biodiversidade-FUNBIO.
Maués, MM, MC Cavalcante, ACS Santos & C Krug, 2018. Brazil nut in the Amazon, pp. 220-225. In: Roubik, DW. (Ed.). The pollination of cultivated plants: A compendium for practitioners. 1ed. Rome, FAO.
Meiners, JM, TL Griswold & OM Carril, 2019. Decades of native bee biodiversity surveys at Pinnacles National Park highlight the importance of monitoring natural areas over time. PLoS ONE, 14: e0207566. DOI: https://doi.org/10.1371/journal.pone.0207566
Michener, CD, 1979. Biogeography of the Bees. Annals of the Missouri Botanical Garden, 66: 277. DOI: https://doi.org/10.2307/2398833
Michener, CD, 2007. The bees of the world, 2nd ed. Baltimore, Johns Hopkins University Press.
Morato, EF, MVB Garcia & LA de O Campos, 1999. Biologia de Centris Fabricius (Hymenoptera, Anthophoridae, Centridini) em matas contínuas e fragmentos na Amazônia Central. Revista Brasileira de Zoologia, 16: 1213-1222. DOI: https://doi.org/10.1590/S0101-81751999000400029
Oliveira, ML de, 1999. Sazonalidade e horário de atividade de abelhas Euglossinae (Hymenoptera, Apidae), em florestas de terra firme na Amazônia Central. Revista Brasileira de Zoologia, 16: 83-90. DOI: https://doi.org/10.1590/S0101-81751999000100003
Oliveira, ML de & LA de O Campos, 1995. Abundância, riqueza e diversidade de abelhas Euglossinae (Hymenoptera, Apidae) em florestas contínuas de terra firme na Amazônia Central, Brasil. Revista Brasileira de Zoologia, 12: 547-556. DOI: https://doi.org/10.1590/S0101-81751995000300009
Oliveira, ML, EF Morato & MVB Garcia, 1995. Diversidade de espécies e densidade de ninhos de abelhas sociais sem ferrão (Hymenoptera, Apidae, Meliponinae) em floresta de terra firme na Amazônia central. Revista Brasileira de Zoologia, 12: 13-24. DOI: https://doi.org/10.1590/S0101-81751995000100004
Oliveira, ML de, 2015. Andrenidae, Apidae, Colletidae, Halictidae, Megachilidae In Catálogo Taxonômico da Fauna do Brasil. PNUD. Available in: <http://fauna.jbrj.gov.br/fauna/faunadobrasil/1295>. [Access: 14.ix.2019].
Oliveira, MM, CI Silva, FB Gomes, MM Maués, ML de Oliveira & C Krug, 2020. Bees, plants and pollen in Central Amazonia - how surrounding areas contribute to pollination of guarana (Paullinia cupana var. sorbilis (Mart.) Ducke), pp. 50-59. In: Silva CI, JN Radaeski, MVN Arena & SG Bauermann (Eds.). Atlas of pollen and plants used by bees. 1ed. Rio Claro, CISE.
Orr, MC, AC Hughes, D Chesters, J Pickering, CD Zhu & JS Ascher, 2021. Global Patterns and Drivers of Bee Distribution. Current Biology, 31: 451-458. DOI: https://doi.org/10.1016/j.cub.2020.10.053
Pinheiro-Machado, C, I Alves-dos-Santos, VL Imperatriz-Fonseca, ADMP Kleinert & FA Silveira, 2002. Brazilian bee surveys: state of knowledge, conservation and sustainable use, p.115-129. In: Kevan P & VL Imperatriz Fonseca (Eds.). Pollinating Bees, The Conservation Link Between Agriculture and Nature. Brasília, Ministério do Meio Ambiente.
R Development Core Team, 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Available in: .
Rondeau, D, B Perry & F Grimard, 2020. The Consequences of COVID-19 and Other Disasters for Wildlife and Biodiversity. Environmental and Resource Economics, 76: 945-961. DOI: https://doi.org/10.1007/s10640-020-00480-7
Sánchez-Bayo, F & KAG Wyckhuys, 2019. Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232: 8-27. DOI: https://doi.org/10.1016/j.biocon.2019.01.020
Schoeninger, K, JLP Souza, C Krug & ML de Oliveira, 2019. Diversity of parasitoid wasps in conventional and organic guarana (Paullinia cupana var. sorbilis) cultivation areas in the Brazilian Amazon. Acta Amazonica, 49: 283-293. DOI: https://doi.org/10.1590/1809-4392201804560
Silveira, FA, GAR Melo & EAB Almeida, 2002. Abelhas brasileiras: sistemática e identificação, 1 Ed. Belo Horizonte, FA Silveira.
Schultz, QS & ACC Valois, 1974. Estudos sobre o mecanismo de floração e frutificação do guaranazeiro. IPAAO (Boletim Técnico 4: 35-36).
Tavares, AM, AL Atroch, FJ Nascimento-Filho, JCR Pereira, JCA Araújo & LAC Moraes, 2005. Cultura do guaranazeiro no Amazonas 4 Ed., pp. 1-40. In: Pereira, JCR (Ed.). Embrapa Amazônia Ocidental - Sistemas de Produção 2. Manaus, Embrapa.
Townes, H., 1972. A light-weight Malaise trap. Entomological News, 83: 239-247.
Downloads
Published
How to Cite
Issue
Section
License
Access is unrestricted and the documentation available on the Creative Commons License (BY) (http://creativecommons.org/licenses/by/4.0/ ).
I declare for proper purposes that the copyright of the submitted text is now licensed in the form of the Creative Commons License, as specified above.
The copyright of the article belongs to the authors
Funding data
-
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Grant numbers Finance Code 0001 -
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Grant numbers 305150/2020-0 -
Empresa Brasileira de Pesquisa Agropecuária
Grant numbers Project 02.16.04.024.00.01.000