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The Science of Nature

, 105:55 | Cite as

Impact of environmental temperatures on mortality, sex and caste ratios in Melipona interrupta Latreille (Hymenoptera, Apidae)

  • Tatiane Becker
  • Pedro Aurélio Costa Lima Pequeno
  • Gislene Almeida Carvalho-Zilse
Original Paper
  • 38 Downloads

Abstract

Temperature is a major driver of biological phenomena, from metabolism to ecological interactions and rates of evolutionary diversification. However, species vary greatly in their thermal tolerance, as well as the temperature under which they perform best. This study aimed to investigate the effect of experimental manipulation of environmental temperatures on the individual mortality and phenotypic composition of colonies of Melipona interrupta. To fulfill these objectives, 30 colonies in equivalent developmental conditions were artificially subjected to different temperatures. Temperatures were monitored by thermo-hygrometers, and immature mortality and sex and caste ratios were observed in brood combs during 14 months. A strong effect of external temperature on immatures was detected on deviations from 28 to 30 °C (the natural average temperature inside the colony), causing an increase in mortality. Likewise, a significant effect of temperature on sex ratio was detected, with male:female ratio decreasing at temperatures below and above 28–30 °C. Lastly, there was no clear evidence for an effect of temperature on caste ratio, although queens appeared to become relatively more frequent at warmer temperatures. The results of this study allow us to conclude that anthropogenic changes, whose effect can be extrapolated to the similar natural changes, that modify the environmental temperatures to which M. interrupta colonies are exposed are likely to compromise their survival, mainly through individual mortality.

Keywords

Thermal response Pollinators Amazon Stingless bees Meliponini 

Notes

Acknowledgments

We are grateful to the anonymous referees for the constructive suggestions. We acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a MSc scholarship to the first author and the Instituto Nacional de Pesquisas da Amazônia (INPA), Graduate Program in Entomology (PPG-Entomologia) for the logistical support.

Funding

We thank the sponsoring agencies FAPEAM and CNPq and CENBAM (Instituto Nacional de Ciência e Tecnologia-Centro de Estudos Integrados da Biodiversidade Amazônica) for the financial support.

Supplementary material

114_2018_1577_MOESM1_ESM.docx (43 kb)
ESM 1 (DOCX 43 kb)

References

  1. Allen AP, Gillooly JF, Savage VM, Brown JH (2006) Kinetic effects of temperature on rates of genetic divergence and speciation. Proc Natl Acad Sci U S A 103(24):9130–9135.  https://doi.org/10.1073/pnas.0603587103 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barbosa-Costa K, Carvalho-Zilse GA (2013) Processo de oviposição da abelha da Amazônia ScaptotrigonaxanthotrichaMoure, 1950. In: Bermúdez EGC, Teles BR, Keppler RF (eds) Entomologia na Amazônia brasileira, 1st edn. Editora INPA, Manaus, pp 91–106Google Scholar
  3. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377.  https://doi.org/10.1111/j.1461-0248.2011.01736.x CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brito DV, Nunes RA, Pequeno PACL, Nunes-Silva CG, Carvalho-Zilse GA (2013) Differential environmental effects on caste allocation in two Amazonian Melipona bees. Apidologie 44(6):666–672.  https://doi.org/10.1007/s13592-013-0215-8 CrossRefGoogle Scholar
  5. Brito DV, Silva CGN, Hasselmann M, Viana LS, Astolfi-Filho S, Carvalho-Zilse GA (2015) Molecular characterization of the gene feminizer in the stingless bee Meliponainterrupta (Hymenoptera: Apidae) reveals association to sex and caste development. Insect Biochem Mol Biol 66:24–30CrossRefPubMedCentralGoogle Scholar
  6. Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2007) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45(3):773–783.  https://doi.org/10.1111/j.1365-2664.2007.01412.x CrossRefGoogle Scholar
  7. Brosi BJ (2009) The complex responses of social stingless bees (Apidae: Meliponini) to tropical deforestation. For Ecol Manag 258(9):1830–1837.  https://doi.org/10.1016/j.foreco.2009.02.025 CrossRefGoogle Scholar
  8. Brown J, Gillooly J, Allen A, Savage V, West G (2004) Toward a metabolic theory of ecology. Ecology 85(7):1771–1789 Retrieved from:http://www.esajournals.org/doi/abs/10.1890/03-9000 CrossRefGoogle Scholar
  9. Brown JC, Albrecht C (2001) The effect of tropical deforestation on stingless bees of the genus Melipona (Insecta: Hymenoptera: Apidae: Meliponini) in central Rondonia, Brazil. J Biogeogr 28:623–634.  https://doi.org/10.1046/j.1365-2699.2001.00583.x CrossRefGoogle Scholar
  10. Carmargo JMF, Kerr WE, Lopes CR (1967) Morfologia externa de Melipona (Melipona) marginata Lepeletier (Hymenoptera, Apidae). Pap Avulsos Zool 20:229–258Google Scholar
  11. Carvalho-Zilse GA, Vilas-Boas HC, Costa KB, Nunes-Silva CG, Souza MT, Fernandes RS (2012) Meliponicultura na Amazônia. INPA, ManausGoogle Scholar
  12. Chown S, Hoffmann A, Kristensen T, Angilletta M, Stenseth N, Pertoldi C (2010) Adapting to climate change: a perspective from evolutionary physiology. Clim Res 43(1):3–15.  https://doi.org/10.3354/cr00879 CrossRefGoogle Scholar
  13. Clusella-Trullas S, Blackburn TM, Chown SL (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am Nat 177(6):738–751.  https://doi.org/10.1086/660021 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Couto RM, Camillo E (2007) Influence of temperature on the immatures mortality of Centris (Heterocentris) analis (Hymenoptera, Apidae, Centridini). Iheringia, Sér Zool 97(1):51–55.  https://doi.org/10.1590/S0073-47212007000100008 CrossRefGoogle Scholar
  15. DeFries RS, Rudel T, Uriarte M, Hansen M (2010) Deforestation driven by urban population growth and agricultural trade in the twenty-first century. Nat Geosci 3:178–181.  https://doi.org/10.1038/ngeo756 CrossRefGoogle Scholar
  16. Deutsch C A, Tewksbury J J, Huey R B, Sheldon K S, Ghalambor C K, Haak D C, Martin P R (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci U S A. Retrieved from: http://www.pnas.org/content/105/18/6668.short
  17. Engels W, Rosenkranz P, Engels E (1995) Thermoregulation in the nest of the Neotropical stingless bee Scaptotrigonapostiça and a hypothesis on the evolution of temperature homeostasis in highly eusocial bees. Stud Neotrop Fauna E30(4):193–205.  https://doi.org/10.1080/01650529509360958 CrossRefGoogle Scholar
  18. Francini IB, Nunes-Silva CG, Carvalho-ZilseG A (2012) Diploid male production of two Amazonian Melipona bees (Hymenoptera: Apidae). Psyche 1:1–7Google Scholar
  19. Heard TA (1999) The role of stingless bees. Annu Ver Entomol 44:183–206.  https://doi.org/10.1146/annurev.ento.44.1.183 CrossRefGoogle Scholar
  20. INMET (2014) http://www.inmet.gov.br. Accessed 5 Nov 2014
  21. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Stocker T F, Qin D, Plattner G K, Tignor M, Allen S K, Boschung J, Nauels a, Xia Y, Bex V, Midgley P M (ed). Cambridge University press, Cambridge, 1535pGoogle Scholar
  22. Jones J, Oldroyd B (2006) Nest thermoregulation in social insects. Adv Insect Physiol 33(06):153–191.  https://doi.org/10.1016/S0065-2806(06)33003-2 CrossRefGoogle Scholar
  23. Kerr WE (1950) Genetic determination of castes in the genus Melipona. Genetics 35(2):143–152 Retrieved from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1209477&tool=pmcentrez&rendertype=abstract PubMedPubMedCentralGoogle Scholar
  24. Kerr WE (1974) Sex determination in bees. III Caste determination and genetic control in Melipona. Insect Soc 21:357–368CrossRefGoogle Scholar
  25. Kerr WE (1996) Biologia e manejo da tiúba: a abelha do Maranhão. EDUFMA, São LuisGoogle Scholar
  26. Kerr WE (1997) Sex determination in honey bees (Apinae and Meliponinae) and its consequences. Braz J Genet 20:601–611CrossRefGoogle Scholar
  27. Kerr WE, Carvalho GA, Nascimento VA (1996) Abelha Uruçu: Biologia, Manejo e Conservação. Fundação Acangaú, Belo HorizonteGoogle Scholar
  28. Kerr WE, Carvalho GA, Coletto-Silva A, Assis MGP (2001) Aspectos Pouco Mencionados da Biodiversidade Amazônica.InBiodiversidade, Pesquisa e Desenvolvimento na Amazônia. Parcerias Estratégicas, Ministério da Ciência e Tecnologia 12:20–41Google Scholar
  29. Kerr WE, Stort AC, Montenegro MJ (1966) Importância de alguns fatores ambientais na determinação das castas no gênero Melipona. An Acad Bras Ciênc 38(1):151–168Google Scholar
  30. Lopes MTR, Barbosa AL, Neto JMV, Pereira FM, Camargo RCR, Ribeiro VQ, Souza BA (2011) Alternativas de sombreamento para apiários. Pesquisa Agropecuária Tropical 41(3):299–305.  https://doi.org/10.5216/pat.v41i3.8919 CrossRefGoogle Scholar
  31. Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios H, McCain CM, McCune AR, McDade L, McPeek M, Near TJ, Price TD, Ricklefs RE, Roy K, Sax DF, Schluter D, Sobel JM, Turelli M (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 10(4):315–331.  https://doi.org/10.1111/j.1461-0248.2007.01020.x CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nogueira-Neto P (1997) Vida e criação de abelhas indígenas sem ferrão. Editora Nogueirapis, São PauloGoogle Scholar
  33. Nunes-Silva CG, Kerr WE, Bonetti AM, Carvalho-Zilse GA (2006) Effect of juvenile hormone III and heat shock in caste determinations in Melipona scutellaris Latreille, 1811 (Hymenoptera, Apidae). Magistra 18(4):277–280Google Scholar
  34. Palmer G, Platts PJ, Brereton T, Chapman JW, Dytham C, Fox R, Pearce-Higgins J, Roy DB, Hill JK, Thomas CD (2017) Climate change, climatic variation and extreme biological responses. Phil Trans R Soc B 372:20160144.  https://doi.org/10.1098/rstb.2016.0144 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37(2006):637–669.  https://doi.org/10.2307/annurev.ecolsys.37.091305.30000024 CrossRefGoogle Scholar
  36. Pereboom JJM, Biesmeijer JC (2003) Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia 137(1):42–50.  https://doi.org/10.1007/s00442-003-1324-2 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0, http://www.R-project.org/ Google Scholar
  38. Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143.  https://doi.org/10.1051/apido:2006026 CrossRefGoogle Scholar
  39. Roubik D, Peralta F (1983) Thermodynamics in nests of two Melipona species in Brasil. Acta Amazon 13(2):453–466 Retrieved from: http://agris.fao.org/agris-search/search.do?recordID=US201302048790 CrossRefGoogle Scholar
  40. Settele J, Bishop J, Potts SG (2016) Climate change impacts on pollination. Nature plants 2(7):16092.  https://doi.org/10.1126/science.aaa4984 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Urban MC (2015) Accelerating extinction risk from climate change. Science 348(6234):571–573.  https://doi.org/10.1038/nplants.2016.9210.1038/nplants.2016.92 CrossRefPubMedGoogle Scholar
  42. Whiting, P W (1943) Multiple Alleles in complementary sex determination of Habrobracon. Genetics 28(5):365–382Google Scholar
  43. Wood SN (2006) Generalized additive models: an introduction with R. Chapman and Hall/CRCGoogle Scholar
  44. Zuur AF, Ieno EM, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto Nacional de Pesquisas da Amazônia (INPA), Programa de Pós-Graduação em Entomologia (PPGENTO)ManausBrazil
  2. 2.Instituto Nacional de Pesquisas da Amazônia (INPA), Coordenação de Biodiversidade (COBIO), Grupo de Pesquisas em Abelhas (GPA)ManausBrazil
  3. 3.Universidade Federal de Roraima (UFRR), Programa de Pós-Graduação em Recursos Naturais (PRONAT)Boa VistaBrazil

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