Orchid bees (Hymenoptera, Apidae, Euglossini) are seasonal in Seasonal Semideciduous Forest fragments, southern Brazil

English

Authors

  • Cleiton Margatto Universidade Federal do Paraná (UFPR), Departamento de Biodiversidade (DBD) - Palotina, PR, Brasil.
  • Vinicius Ortega Berno Eastern New Mexico University (ENMU)
  • Rodrigo Barbosa Gonçalves Universidade Federal do Paraná (UFPR), Departamento de Zoologia (DZOO) - Curitiba, PR, Brasil http://orcid.org/0000-0001-5623-0938
  • Luiz Roberto Ribeiro Faria Jr. Universidade Federal da Integração Latino-Americana (UNILA), Instituto Latino-americano de Ciências da Vida e da Natureza (ILACVN) - Foz do Iguaçu, PR, Brasil http://orcid.org/0000-0002-7214-106X

DOI:

https://doi.org/10.11606/1807-0205/2019.59.07

Keywords:

Annual cycles, Insect, Life-cycle, Neotropical, Seasonality

Abstract

Seasonal fluctuations in the abundance of orchid bees have already been reported. The variations in population dynamics may be expected to occur in more predictable and pronounced manners in environments with a clear distinction between rainy and dry seasons, where climatic variables are regarded to be good predictors of populational patterns. The main goal of this paper is to investigate the seasonality of males of orchid bees in fragments of Seasonal Semideciduous Forest in southern Brazil. Data comprise bait samples from five one-year periods on four forest fragments. The seasonality of species abundance was tested with circular statistics. Results suggest two phenological patterns, one for Eufriesea violacea (Blanchard), Eulaema nigrita Lepeletier and Euglossa cordata (Linnaeus), whose abundances are concentrated in late spring and early-middle summer and another for Euglossa fimbriata Moure with a tendency to be collected in middle-late summer and early autumn. These patterns are discussed, as well the possible driven factors, (i) the species life cycle and nesting behavior, (ii) synchrony with resource, and (iii) climate. We can postulate an important impact of climate change in local euglossine assemblage due to the small populations and marked seasonality.

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Author Biographies

  • Cleiton Margatto, Universidade Federal do Paraná (UFPR), Departamento de Biodiversidade (DBD) - Palotina, PR, Brasil.

    Avenida Pioneiro, 2.153, Jardim Dallas, CEP 85950‑000, Palotina, PR, Brasil.

  • Vinicius Ortega Berno, Eastern New Mexico University (ENMU)

    1500 S Avenue K, 88130, Portales, NM, USA.

  • Rodrigo Barbosa Gonçalves, Universidade Federal do Paraná (UFPR), Departamento de Zoologia (DZOO) - Curitiba, PR, Brasil

    Avenida Coronel Francisco Heráclito dos Santos, 100, Jardim das Américas, CEP 81531‑980, Curitiba, PR, Brasil.

  • Luiz Roberto Ribeiro Faria Jr., Universidade Federal da Integração Latino-Americana (UNILA), Instituto Latino-americano de Ciências da Vida e da Natureza (ILACVN) - Foz do Iguaçu, PR, Brasil

    Avenida Tarquínio Joslin dos Santos, 1.000, Loteamento Universitário das Américas, CEP 85870‑901, Foz do Iguaçu, PR, Brasil.

References

Abrahamczyk, S.; Gottleuber, P. & Kessler, M. 2012. Seasonal changes in odour preferences by male euglossine bees (Hymenoptera: Apidae) and their ecological implications. Apidologie, 43: 212‑217.

Ackerman, J.D. 1983. Diversity and seasonality of male euglossine bees (Hymenoptera: Apidae) in central Panamá. Ecology, 64: 274‑283.

Aguiar, W.M. & Gaglianone, M.C. 2008. Comunidade de abelhas Euglossina (Hymenoptera: Apidae) em remanescentes de mata estacional semidecidual sobre tabuleiro no estado do Rio de Janeiro. Neotropical Entomology, 37: 118‑125.

Aguiar, W.M. & Gaglianone, M.C. 2012. Euglossine bee communities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae). Revista Brasileira de Entomologia, 56: 210‑219.

Andrade-Silva, A.C.R.; Nemésio, A.; de Oliveira F.F. & Nascimento, F.S. 2012. Spatial-Temporal Variation in Orchid Bee Communities (Hymenoptera: Apidae) in Remnants of Arboreal Caatinga in the Chapada Diamantina Region, State of Bahia, Brazil. Neotropical Entomology, 41: 296‑305.

Armbruster, W.S. 1993. Within-habitat heterogeneity in baiting samples of male euglossine bees: possible causes and implications. Biotropica, 25: 122‑128.

Augusto, S.C. & Garófalo, C.A. 2009. Bionomics and sociological aspects of Euglossa fimbriata (Apidae, Euglossini). Genetics and Molecular Research, 8: 525‑538.

Augusto, S.C. & Garófalo, C.A. 2011. Task allocation and interactions among females in Euglossa carolina nests (Hymenoptera, Apidae, Euglossini). Apidologie, 42: 162‑173.

Batschelet, E. 1981. Circular statistics in biology. London, Academic Press.

Campos, L.A.O.; Silveira, F.A.; Oliveira, M.L.; Abrantes, C.V.M.; Morato, E.F. & Melo, G.A.R. 1989. Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Revista Brasileira de Zoologia, 6: 621‑626.

Castro, M.M.N.; Garófalo, C.A.; Serrano, J.C. & Silva, C.I. 2013. Temporal variation in the abundance of orchid bees (Hymenoptera: Apidae) in a Neotropical hygrophilous forest. Sociobiology, 60: 405‑412.

Danks, H.V. 2007. The elements of seasonal adaptations in insects. The Canadian Entomologist, 139: 1‑44.

Dodson, C.H.; Dressler, R.L.; Hills, H.G.; Adams, R.M. & Williams, N.H. 1969. Biologically active compounds in orchid fragrances. Science, 164: 1243‑1249.

Dressler, R.L. 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology and Systematics, 13: 373‑394.

Essinger, L.N. 2005. Euglossini (Apidae, Hymenoptera) no sul de Santa Catarina. MSc. Dissertation. Criciúma, UNESC. 63p.

Faria, L.R.R. & Melo, G.A.R. 2007. Species of Euglossa (Glossura) in the Brazilian Atlantic forest, with taxonomic notes on Euglossa stellfeldi Moure (Hymenoptera, Apidae, Euglossina). Revista Brasileira de Entomologia, 51: 275‑284.

Farzan, S. & Yang, L.H. 2018. Experimental shift in phenology affects fitness, foraging, and parasitism in a native solitary bee. Ecology, 99(10): 2187‑2195. DOI

Forrest, J.R.K. 2015. Plant – pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations? Oikos, 124: 4‑13.

Freiria, G.A.; Garófalo, C.A. & Del Lama, M.A. 2017. The primitively social behavior of Euglossa cordata (Hymenoptera, Apidae, Euglossini): a view from the perspective of kin selection theory and models of reproductive skew. Apidologie, 48: 523‑532.

Garófalo, C.A. 1985. Social structure of Euglossa cordata nests (Hymenoptera: Apidae: Euglossini). Entomologia Generalis, 11: 77‑83.

Garófalo, C.A.; Camillo, E. & Serrano, J.C. 1993. Utilization of trap nests by Euglossini species (Hymenoptera: Apidae). Revista Brasileira de Biologia, 53: 177‑187.

Gaston, K.J. 2009. Geographic range limits: achieving synthesis. Proceedings of the Royal Society B, 276: 1395‑1406.

Gonçalves, R.B.; Sydney, N.V.; Oliveira, P.S. & Artmann, N.O. 2014a. Bee and wasp responses to a fragmented landscape in southern Brazil. Journal of Insect Conservation, 18: 1193‑1201.

Gonçalves, R.B.; Scherer, V.L. & Oliveira, P.S. 2014b. The orchid bees (Hymenoptera, Apidae, Euglossina) in a forest fragment from western Paraná state, Brazil. Papéis Avulsos de Zoologia, 54: 63‑68.

Instituto Brasileiro de Geografia e Estatística (IBGE). 2018. Brasil em síntese. Available at: https://cidades.ibge.gov.br. Accessed in: 17/01/2019.

Janzen, D.H.; Devries, P.J.; Heggins, M.L. & Kimsey, L.S. 1982. Seasonal and site variation in Costa Rican euglossine bees at chemical baits in lowland deciduous and evergreen forests. Ecology, 63: 66‑74.

Kimsey, L.S. 1982. Systematics of bees of the genus Eufriesea. University of California Publications in Entomology, 95: 1‑125.

Knoll, F.R. 2016. Variation in the abundance of Neotropical bees in an unpredictable seasonal environment. Neotropical Entomology, 45: 129‑138.

Kovach, W.L. 2011. Oriana: Circular Statistics for Windows (version 4.0). Pentraeth, Kovach Computer Services.

Marchioretto, M.A.; Mauhs, J. & Budke, J.C. 2007. Fenologia de espécies arbóreas zoocóricas em uma floresta psamófila no sul do Brasil. Acta Botanica Brasilica, 21: 193‑201.

Marinoni, R.C. & Ganho, N.G. 2003. Sazonalidade de Nyssodrysina lignaria (Bates) (Coleoptera, Cerambycidae, Lamiinae), no estado do Paraná, Brasil. Revista Brasileira de Zoologia, 20: 141‑152.

Marques, M.C.M.; Roper, J.J. & Salvalaggio, A.P.B. 2004. Phenological patterns among plant life forms in a subtropical forest in Southern Brazil. Plant Ecology, 173: 203‑213.

Mateus, S.; Andrade, A.C.R. & Garófalo, C.A. 2015. Diversity and temporal variation in the orchid bee community (Hymenoptera: Apidae) of a remnant of a Neotropical seasonal semi-deciduous forest. Sociobiology, 62(4): 571‑577.

Mikich, S.B. & Silva, S.M. 2001. Composição florística e fenologia das espécies zoocóricas de remanescentes de Floresta Estacional Semidecidual no centro-oeste do Paraná, Brasil. Acta Botanica Brasílica, 15: 89‑113.

Morellato, L.P.C.; Talora, D.C.; Takahasi, A.; Bencke, C.C.; Romera, E.C. & Zipparro, V.B. 2000. Phenology of Atlantic rain forest trees: a comparative study. Biotropica, 32: 811‑823.

Moure, J.S.; Melo, G.A.R. & Faria Jr., L.R.R. 2007. Euglossini Latreille, 1802. In: Moure, J.S.; Urban, D. & Melo, G.A.R. (Eds.). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Curitiba, Sociedade Brasileira de Entomologia. p. 214‑255.

Nemésio, A. 2009. Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, 2041: 1‑242.

Nemésio, A. & Silveira, F.A. 2006. Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlantic Forest in southeastern Brazil. Neotropical Entomology, 35: 313‑323.

Oliveira, R.; Pinto, C.E. & Schlindwein, C. 2015. Two common species dominate the species-rich Euglossine bee fauna of an Atlantic Rainforest remnant in Pernambuco, Brazil. Brazilian Journal of Biology, 75: S1‑S8.

Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37: 637‑669.

Pedron, I.T.; Mariani, K.L.; Farias, J.L.R. & Rossetto, A. 2013. Comportamento do clima de Palotina, PR de 1973 a 2010. Scientia Agraria Paranaensis, 12: 411‑419.

Pereira-Martins, S.R. 1991. Biologia de Eulaema nigrita. 2. Atividades nidais. Papéis Avulsos de Zoologia, 37: 237‑243.

Peruquetti, R.C. & Campos, L.A.O. 1997. Aspectos da biologia de Euplusia violacea (Blanchard) (Hymenoptera, Apidae, Euglossini). Revista Brasileira de Zoologia, 14: 91‑97.

Peruquetti, R.C.; Campos, L.A.O.; Coelho, C.D.P.; Abrantes, C.V.M. & Lisboa, L.C.O. 1999. Abelhas Euglossini (Apidae) de áreas de Mata Atlântica: abundância, riqueza e aspectos biológicos. Revista Brasileira de Zoologia, 16: 101‑118.

Powell, J.A. & Logan, J.A. 2005. Insect seasonality: circle map analysis of temperature-driven life cycles. Theoretical Population Biology, 67: 161‑179.

Ramírez, S.R.; Roubik, D.W.; Skov, C. & Pierce, N.E. 2010. Phylogeny, diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae). Biological Journal of the Linnean Society, 100: 552‑572.

Rebêlo, J.M.M. & Garófalo, C.A. 1991. Diversidade e sazonalidade de machos de Euglossini (Hymenoptera, Apidae) e preferência por iscas odores em um fragmento de floresta no sudeste do Brasil. Revista Brasileira de Biologia, 51: 787‑799.

Rebêlo, J.M.M. & Garófalo, C.A. 1997. Comunidades de machos de Euglossinae (Hymenoptera, Apidae) em matas semidecíduas do nordeste do estado de São Paulo. Anais da Sociedade Entomológica do Brasil, 26: 243‑256.

Rebêlo, J.M.M. & Moure, J.S. 1996. As espécies de Euglossa Latreille do nordeste de São Paulo (Apidae, Euglossinae). Revista Brasileira de Zoologia, 12: 445‑466.

Richards, L.A. & Windsor, D.M. 2007. Seasonal variation of arthropod abundance in gaps and the understorey of a lowland moist forest in Panama. Journal of Tropical Ecology, 23: 169‑176.

Riedel, R.; Marinoni, R.C. & Martins-Opolis, N. 2008. Spatio-temporal trends of insect communities in southern Brazil. Journal of Entomology, 5: 369‑380.

Rocha-Filho, L.C. & Garófalo, C.A. 2014. Phenological patterns and preferences for aromatic compounds by male euglossine bees (Hymenoptera, Apidae) in two coastal ecosystems of the Brazilian Atlantic forest. Neotropical Entomology, 43: 9‑20.

Roubik, D.W. 1989. Ecology and natural history of tropical bees. Cambridge, Cambridge University Press, 528p.

Roubik, D.W. & Ackerman, J.D. 1987. Long-term ecology of euglossine orchid-bees (Apidae: Euglossini) in Panama. Oecologia, 73: 321‑333.

Roubik, D.W. & Hanson, P.E. 2004. Orchid bees of tropical America: biology and field guide. San Jose, INBIO. 370p.

Roubik, D.W. & Michener, C.D. 1980. The seasonal cycle and nests of Epicharis zonata, a bee whose cells are below the wet-season water table (Hymenoptera, Anthophoridae). Biotropica, 12: 56‑60.

Sakagami, S.F.; Laroca, S. & Moure, J.S. 1967. Wild bees biocenotics in São José dos Pinhais (PR), South Brazil – preliminary report. Journal of the Faculty of Sciences of the Hokkaido University, Series 6, Zoology, 19: 253‑91.

Santos, M.L. & Garófalo, C.A. 1994. Nesting biology and nest re-use of Eulaema nigrita (Hymenoptera: Apidae, Euglossini). Insectes Sociaux, 41: 99‑110.

Schrottky, C. 1907. Contribución al conocimiento de los himenópteros del Paraguay. Anales de Ciêntificos Paraguayos, 7: 1‑78.

Schürch, R.; Accleton, C. & Field, J. 2016. Consequences of a warming climate for social organisation in sweat bees. Behavioral Ecology and Sociobiology, 70: 1131‑1139.

Silva, F.S. & Rebêlo, J.M.M. 2002. Population dynamics of euglossine bees (Hymenoptera, Apidae) in an early second-growth forest of Cajual Island, in the state of Maranhão, Brazil. Brazilian Journal of Biology, 62: 15‑23.

Soares, A.A.; Campos, L.A.O.; Vieira; M.F. & Melo, G.A.R. 1989. Relações entre Euglossa (Euglossella) mandibularis Friese, 1899 (Hymenoptera, Apidae, Euglossini) e Cyphomandra calycina (Solanaceae). Ciência e Cultura, 41(9): 903‑905.

Sobral-Souza, T.; Francini, R.B.; Guimarães, M. & Benson, W.W. 2015. Short-dynamics reveals seasonality in a subtropical Heliconius butterfly. Journal of Insects, 2015(ID761058): 1‑5. Available in: https://www.hindawi.com/journals/insects/2015/761058.

Sofia, S.H. & Suzuki, K.M. 2004. Comunidades de machos de abelhas Euglossina (Hymenoptera: Apidae) em fragmentos florestais no sul do Brasil. Neotropical Entomology, 33: 693‑702.

Sofia, S.H.; Santos, A.M. & Silva, C.R.M. 2004. Euglossine bees (Hymenoptera, Apidae) in a remnant of Atlantic Forest in Paraná state, Brazil. Iheringia, Série Zoologia, 94: 217‑222.

Sydney, N.V. & Gonçalves, R.B. 2015. Is the capture success of orchid bees (Hymenoptera, Apoidea) influenced by diferent baited trap designs? A case study from southern Brazil. Revista Brasileira de Entomologia, 59: 34‑38.

Sydney, N.V.; Gonçalves, R.B. & Faria, L.R.R. 2010. Padrões espaciais na distribuição de abelhas Euglossina (Hymenoptera, Apidae) da região Neotropical. Papéis Avulsos de Zoologia, 50: 667‑679.

Tauber, M.J.; Tauber, C.A. & Masaki, S. 1986. Seasonal adaptations of insects. New York, Oxford University Press. 411p.

Turchin, P.; Taylor, A.D. & Reeve, J.D. 1999. Dynamical role of predators in population cycles of a forest insect: an experimental test. Science, 285: 1068‑1071.

Uehara-Prado, M. & Garófalo, C.A. 2006. Small-scale elevational variation in the abundance of Eufriesea violacea (Blanchard) (Hymenoptera: Apidae). Neotropical Entomology, 35: 446‑451.

Veloso, H.P.; Rangel, A.L.R. & Lima, J.C.A. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. Rio de Janeiro, IBGE‑DERMA.

Visser, M.E.; Caro, S.P.; van Oers, K.; Schaper, S.V. & Helm, B. 2010. Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philosophical Transactions of the Royal Society B: Biological Sciences, 365: 3113‑3127. DOI

Wittmann, D.; Radtke, R.; Hoffmann, M. & Blochstein, B. 1989. Seasonality and seasonal changes in preferences for scent baits in Euplusia violacea in Rio Grande do Sul, Brazil (Hymenoptera, Apidae, Euglossini). Entomologia Generalis, 14: 217‑221.

Wolda, H. 1978. Seasonal fluctuations in rainfall, food and abundance of tropical insects. Journal of Animal Ecology, 47: 369‑381.

Wolda, H. 1980. Seasonality of tropical insects. I. Leafhoppers (Homoptera) in Las Cumbres, Panama. Journal of Animal Ecology, 49: 277‑290.

Wolda, H. 1988. Insect seasonality: why? Annual Review of Ecology and Systematics, 19: 1‑18.

Zar, J.H. 1996. Biostatistical analysis. 3. ed. New Jersey, Prentice-Hall International Editions.

Zucchi, R.; Sakagami, F. & Camargo, J.M.F. 1969. Biological observations on a Neotropical parasocial bee, Eulaema nigrita, with a review of the biology of Euglossinae: a comparative study. Journal of the Faculty of Sciences of the Hokkaido University, Series 6, Zoology, 17: 271‑380.

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2019-03-13

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How to Cite

Margatto, C., Berno, V. O., Gonçalves, R. B., & Faria Jr., L. R. R. (2019). Orchid bees (Hymenoptera, Apidae, Euglossini) are seasonal in Seasonal Semideciduous Forest fragments, southern Brazil: English. Papéis Avulsos De Zoologia, 59, e20195907. https://doi.org/10.11606/1807-0205/2019.59.07