Bees from an Island in the Delta of the Americas (Maranhão state, Brazil) and their Floristic Interactions
DOI:
https://doi.org/10.13102/sociobiology.v68i3.5783Keywords:
Restinga, floral visitors, floral resources, apifauna, species checklistAbstract
Surveys of the bee fauna on islands are scarce due to the difficult access to the study area. Thus, the current study intended to establish the species of bees present in an island of the Delta of the Americas, called Grande do Paulino, Tutóia, Maranhão. Together with the bees, the plants visited by these insects were recorded, in order to document the relationships between these organisms. Between July 2017 and June 2018, once a month, 1,095 individuals, distributed in 16 tribes, 30 genera, and 48 species, were collected with active (entomological net) and passive (bowl traps) sampling methods. Data from plants and their visiting bees are presented in an interaction network in the form of a bipartite graph, showing Xylocopa cearensis as the most collected bee species, and Chamaecrista ramosa as the most visited plant by bees. In addition to providing information about the bee fauna of the state of Maranhão and, consequently, from the Brazilian northeast, this study explores the apifauna of a place never before explored and, because it is an island, of difficult access, also providing information about the floristic interactions of these insects.
Downloads
References
Aguiar, C. M. L., Gaglianone, M. C. (2003) Nesting biology of Centris (Centris aenea) Lepeletier (Hymenoptera, Apidae, Centridini). Revista Brasileira de Zoologia, 20: 601-606. https://doi.org/10.1590/S0101-81752003000400006
Aguiar, W. M., Gaglianone, M. C. (2012) Euglossine bee comunities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae). Revista Brasileira de Entomologia, 56: 210-219. https://doi.org/10.1590/S0085-56262012005000018
Albuquerque, P. M. C., Camargo, J. M. F., Mendonça, J. A. C. (2007) Bee community of a beach dune ecosystem on Maranhão Island, Brazil. Brazilian Archives of Biology and Technology, 50: 1005-1018. https://doi.org/10.1590/S1516-89132007000700012
Albuquerque, P. M. C., Ferreira, R. G., Rêgo, M. M. C., Santos, C. S., Brito, C. M. S. (2001) Levantamento da fauna de abelhas silvestres (Hymenoptera, Apoidea) na região da “Baixada Maranhense”: Vitória do Mearim, MA, Brasil. Acta Amazonica, 31: 419-430.
Almasri, H., Tavares, D. A., Pioz, M., Sené, D., Tchamitchian, S., Cousin, M., Brunet, J.-L., Belzunces, L. P. (2020) Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicology and Environmental Safety, 203: 111013. https://doi.org/10.1016/j.ecoenv.2020.111013
Almeida, R. P. S., Arruda, F. V., Silva, D. P., Coelho, B. W. T. (2019) Bees (Hymenoptera, Apoidea) in an ecotonal Cerrado-Amazon region in Brazil. Sociobiology, 66: 457–466. http://dx.doi.org/10.13102/sociobiology.v66i3.3463
Almeida‐Neto, M., Guimarães, P., Guimarães, P. R., Loyola, R. D., Ulrich, W. (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos, 117: 1227-1239. https://doi.org/10.1111/j.0030-1299.2008.16644.x
Alvares, C. A., Stape, J.L., Sentelhas, P. C., Gonçalves, J. L. M., Sparovek, G. (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22: 711–728. https://dx.doi.org/10.1127/0941-2948/2013/0507
Bascompte, J., Jordano, P., Melián, C. J., Olesen J. M. (2003) The nested assembly of plant–animal mutualistic networks. PNAS, 100: 9383–9387. https://doi.org/10.1073/pnas.1633576100
Colwell, R. K. (2006) EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.2. http://viceroy.eeb.uconn.edu/estimates. (accessed date: 12 August, 2020)
Dormann, C. F., Fruend, J., Gruber, B. (2018) Visualising bipartite networks and calculating some (ecological) indices. Version 2.11. https://github.com/biometry/bipartite. (accessed date: 12 August, 2020)
Eliash, N., Mikheyev, A. (2020) Varroa mite evolution: a neglected aspect of worldwide bee collapses? Current Opinion in Insect Science, 39: 21–26. https://doi.org/10.1016/j.cois.2019.11.004
Faita, M. R., Cardozo, M. M., Amandio, D. T. T., Orth, A. I., Nodari, R. O. (2020). Glyphosate-based herbicides and Nosema sp. microsporidia reduce honey bee (Apis mellifera L.) survivability under laboratory conditions. Journal of Apicultural Research, 59: 332–342. https://doi.org/10.1080/00218839.2020.1736782
Gerling, D., Velthuis, H. H. W., Hefetz, A. (1989) Bionomics of the large carpenter bees of the genus Xylocopa. Annual Review of Entomology, 34: 163–190. https://doi.org/10.1146/annurev.en.34.010189.001115
Gostinski, L. F., Carvalho, G. C. A., Rêgo, M. M. C., Albuquerque, P. M. C. (2016) Species richness and activity pattern of bees (Hymenoptera, Apidae) in the restinga area of Lençóis Maranhenses National Park, Barreirinhas, Maranhão, Brazil. Revista Brasileira de Entomologia, 60: 319–327. https://doi.org/10.1016/j.rbe.2016.08.004
Gottsberger, G., Silberbauer-Gottsberger, I. (1988) Evolution of flower structures and pollination in Neotropical Cassiinae (Caesalpiniaceae) species. Phyton, 28: 293–320
Grimaldi, D. (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous. Annals of the Missouri Botanical Garden, 86: 373–406. doi: 10.2307/2666181
Guimarães Jr, P. R., Guimarães, P. (2006) Improving the analyses of nestedness for large sets of matrices. Environmental Modelling & Software, 21: 1512–1513. https://doi.org/10.1016/j.envsoft.2006.04.002
Hammer, Ø., Harper, D. A. T., Ryan, P. D. (2013) Past: Paleontological Statiscs Software Package for Educationand Data Analysis. Paleontologia Electronica. https://palaeo-electronica.org/2001_1/past/issue1_01.htm. (accessed date: 12 August, 2020)
Kamke, R., Zillikens, A., Steiner, J. (2011) Species richness and seasonality of bees (Hymenoptera, Apoidea) in a restinga area in Santa Catarina, southern Brazil. Studies on Neotropical Fauna and Environment, 46: 35–48. https://doi.org/10.1080/01650521.2010.538561
Krug, C., Alves-dos-Santos, I. (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. http://dx.doi.org/10.1590/S1519-566X2008000300005
Lewinsohn, T. W., Loyola, R. D., Prado, P. I. (2006) Matrizes, redes e ordenações: a detecção de estrutura em comunidades interativas. Oecologia Brasiliensis, 10: 90-104. https://doi.org/10.4257/oeco.2006.1001.06
Lopes, M. T. R., Reis, A. S., Souza, B. A., Pereira, F. M., Neves, L. S. M. L., Pereira, L. A., Rocha, F. S. B., Vieira Neto, J. M. (2010) Levantamento da fauna e plantas apícolas na Embrapa Meio-Norte, em Teresina, PI. Boletim de Pesquisa e Desenvolvimento. Teresina: Embrapa Meio-Norte, 34 p
Lorenzon, M. C. A., Matrangolo, C. A. R., Schoereder, J. H. (2003) Flora visitada pelas abelhas eussociais (Hymenoptera, Apidae) na Serra da Capivara, em Caatinga do Sul do Piauí. Neotropical Entomology, 32: 27–36. https://doi.org/10.1590/S1519-566X2003000100004
Madeira-da-Silva, M. C., Martins, C. F. (2003) Abelhas (Hymenoptera, Apoidea apiformes) de uma área de Restinga, Paraíba, Nordeste do Brasil: Abundância, diversidade e sazonalidade. Revista Nordestina de Biologia, 17: 75–90.
Mendes, F. N., Rêgo, M. M. C., Albuquerque, P. M. C. (2011) Fenologia e biologia reprodutiva de duas espécies de Byrsonima Rich. (Malpighiaceae) em área de Cerrado no Nordeste do Brasil. Biota Neotropica, 11: 103–115.
Michener, C. D. (2007) The Bees of the World. Baltimore: The Johns Hopkins University Press, 953 p
Mouga, D. M. D. S., Nogueira-Neto, P., Warkentin, M., Feretti, V., Dec, E. (2015) Comunidade de abelhas (Hymenoptera, Apidae) e plantas associadas em área de mata atlântica em São Francisco do Sul, Santa Catarina, Brasil. Acta Biológica Catarinense, 2: 12–31. http://dx.doi.org/10.21726/abc.v2i1.195
Moure, J. S., Urban, D. & Melo, G. A. R. (Orgs). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. http://www.moure.cria.org.br/catalogue. (accessed date: 12 August, 2020)
Moure, J. S., Urban, D., Melo, G. A. R. (2007) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Curitiba: Sociedade Brasileira de Entomologia,1058 p
Neves Jr, C. L., Barros, H., Rêgo, M. (2020). First record of Centris hyptidis Ducke, 1908 (Hymenoptera: Apidae: Centridini) in State of Maranhão, Brazil. Entomological Communications, 2: ec02009. https://doi.org/10.37486/2675-1305.ec02009
Olesen, J. M., Bascompte, J., Dupont, Y. L., Jordano, P. (2006) The smallest of all worlds: pollination networks. Journal of Theoretical Biology, 240: 270-276. https://doi.org/10.1016/j.jtbi.2005.09.014
Oliveira, F. S., Mendonça, M. W. A., Vidigal, M. C. S., Rêgo M. M. C., Albuquerque, P. M. C. (2010) Comunidade de abelhas (Hymenoptera, Apoidea) em ecossistema de dunas na Praia de Panaquatira, São José de Ribamar, Maranhão, Brasil. Revista Brasileira de Entomologia, 54: 82–90. https://doi.org/10.1590/S0085-56262010000100010
Peixoto, A. L., Maia, L. C. (2013) Manual de Procedimentos para Herbários. INCT-Herbário virtual para a Flora e os Fungos. Recife: Editora Universitária UFPE, 95 p
Pigozzo, C. M., Viana, B. F. (2010) Estrutura da rede de interações entre flores e abelhas em ambiente de caatinga. Oecologia Australis, 14: 100–114. doi:10.4257/oeco.2010.1401.04
Pinheiro-Machado, C., Silveira, F. A. (2006) Surveying and monitoring of pollinators in natural landscapes and in cultivated fields. In: Imperariz-Fonseca, V. L., Saraiva, A. M., De Jong, D. (Eds.) Bees as pollinators in Brazil: Assessing the status and suggesting best practices (pp. 25-37). Ribeirão Preto: Holos.
Rêgo, M. M. C., Albuquerque, P. M. C. (2012) Biodiversidade de abelhas em zonas de transição no Maranhão. In: Ribeiro MF (Ed.) III Semana dos Polinizadores: palestras e resumos (pp. 36-57). Petrolina: Embrapa Semi-Árido, 249
Rêgo, M. M. C., Albuquerque, P. M. C. (1989) Comportamento das abelhas visitantes de murici, Byrsonima crassifolia (L.) Kunth, Malpighiaceae. Boletim do Museu Paraense Emílio Goeldi. - Série Zoologia, 5: 179-193.
Rodarte, A. T. A., Silva, F. O., Viana, B. F. (2008) A flora melitófila de uma área de dunas com vegetação de caatinga, Estado da Bahia, Nordeste do Brasil. Acta Botanica Brasilica, 22: 301-312. https://doi.org/10.1590/S0102-33062008000200001
Roubik, D. W. (1989) Ecology and natural history of tropical bees. New York: Cambridge University Press, 514 p
Sakagami, S. F., Laroca, S., Moure, J. S. (1967) Wild bee biocenotics in São José dos Pinhais (PR), South Brazil: preliminary report. Journal of the Faculty of Science, Hokkaido University. Series 6, Zoology, 16: 253-291. http://hdl.handle.net/2115/27447
Santos, A. J. S. (2003) Estimativas de riqueza em espécies. In: Cullen Jr, L., Valdares-Padua, C., Rudran, R. (Eds.) Métodos de estudos em biologia da conservação e manejo da vida silvestre (pp 19-41). Curitiba: UFPR.
Schlindwein, C., Schlumpberger, B., Wittmann, D., Moure, J. S. (2003) O gênero Xylocopa Latreille no Rio Grande do Sul, Brasil (Hymenoptera, Anthophoridae). Revista Brasileira de Entomologia, 47: 107–118. https://doi.org/10.1590/S0085-56262003000100016
Silveira, F. A., Melo, G. A. R., Almeida, E. A. B. (2002) Abelhas Brasileiras: Sistemática e Identificação. Belo Horizonte, 253 p
Somavilla, A., Schoeninger, K., Nogueira, D. S., Kohler, A. (2018) Diversidade de abelhas (Hymenoptera: Apoidea) e visitação floral em uma área de Mata Atlântica no Sul do Brasil. EntomoBrasilis, 11: 191-200. https://doi.org/10.12741/ebrasilis.v11i3.800
Viana, B. F., Alves-dos-Santos, I. (2002) Bee diversity of the coastal sand dunes of Brazil. In: Kevan, P. G., Imperatriz-Fonseca, V. L. (Eds.) Pollinating bees: the conservation link between agriculture and nature (pp 135-153). Brasília: MMA
Viana, B. F., Kleinert, A. M. P. (2006) Structure of bee-flower system in the coastal sand dune of Abaeté, northeastern Brazil. Revista Brasileira de Entomologia, 50: 53–63. https://doi.org/10.1590/s0085-56262006000100008
Viana, B. F., Kleinert, A. M. P., Silva, F. O. (2002) Ecologia de Xylocopa (Neoxylocopa) cearensis (Hymenoptera, Anthophoridae) nas dunas litorâneas de Abaeté, Salvador, Bahia. Iheringia. Série Zoologia, 92: 47–57. https://doi.org/10.1590/S0073-47212002000400007
Viana, T. A., Lourenço, A. P. (2020) Surveys of the bee (Hymenoptera: Apiformes) community in a Neotropical savanna using pan traps. Papéis Avulsos de Zoologia, 60: 1–12. https://doi.org/10.11606/1807-0205/2020.60.31
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Carlos Luis Neves Jr., Harryson Correa Barros, Maira Rodrigues Diniz, Bruna Emanuele Freire Correia, Luciano André Chaves Ferreira, Albeane Guimarães Silva, Eduardo Bezerra de Almeida Jr., Márcia Maria Correa Rêgo

This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).