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Vol. 12 No. 2 (2018)

Vegetable section

Interaction between biological and chemistry fungicides and tomato pollinators

https://doi.org/10.17584/rcch.2018v12i2.7690

Published 2018-09-20

  • Carlos de Melo e Silva-Neto
    • ,
  • Anna Clara Chaves Ribeiro
    • ,
  • Flaviana Lima Gomes
    • ,
  • Jordana Guimarães Neves
    • ,
  • Aniela Pilar Campos de Melo
    • ,
  • Francine Neves Calil
    • ,
  • Abadia dos Reis Nascimento
    • ,
  • Edivani Villaron Franceschinelli

Carlos de Melo e Silva-Neto
Instituto Federal de Goiás (IFG),Laboratório de Sementes e Coleções Biológicas, Goias-GO

Anna Clara Chaves Ribeiro
Universidade Federal de Goiás, Instituto de Ciências Biológicas, Goiânia-GO

Flaviana Lima Gomes
Universidade Federal de Goiás, Instituto de Ciências Biológicas, Laboratório de Biologia Reprodutiva de Plantas, Goiânia-GO

Jordana Guimarães Neves
Universidade Federal de Goiás, Escola de Agronomia, Goiânia-GO

Aniela Pilar Campos de Melo
Instituto Federal Goiano, Campus Avançado Cristalina, Cristalina-GO

Francine Neves Calil
Universidade Federal de Goiás, Escola de Agronomia, Setor de Engenharia Florestal, Goiânia-GO

Abadia dos Reis Nascimento
Universidade Federal de Goiás, Escola de Agronomia, Goiânia-GO

Edivani Villaron Franceschinelli
Universidade Federal de Goiás, Instituto de Ciências Biológicas, Laboratório de Biologia Reprodutiva de Plantas, Goiânia-GO

Abstract

The use of agrochemicals is harmful to bees visiting agricultural crops, reducing production gains from pollination, but the effect of fungicides on these bees is not known. The objective of this study was to verify the effect of bee visitation influenced by different fungicides on the tomato crop and on the deposition of pollen grains on the stigma, number of seeds, mass and fruit size. The experiment was conducted with 10 treatments: (T1) control treatment, without application of agrochemicals; (T2 and T3) Bacillus subtilis in different application frequencies; (T4) copper hydroxide; (T5) B. subtilis and copper hydroxide; (T6) acibenzolar-S-methyl; (T7) (trifloxystrobin+tebuconazole) and B. subtilis; (T8) copper hydroxide+Mancozeb; (T9) propineb+(trifloxystrobin+ tebuconazole); (T10) (trifloxystrobin+tebuconazole)+B. subtilis+copper hydroxide. The presence of the pollination mark on the flower, the pollen load of the stigmas, the number of seeds per fruit, and the size and mass of the fruits were determined in each treatment. Subsequently, the mortality rate of Melipona quadrifasciata (Hymenoptera, Apidae) exposed to four fungicides (trifloxystrobin+tebuconazole; manganese and zinc; copper hydroxide; Bacillus subtilis) was estimated. The mortality rate of M. quadrifasciata over 24 h of evaluation was higher in the treatments with copper hydroxide and trifloxystrobin+tebuconazole (75 and 50%, respectively). The mortality rate was lower in the treatments with manganese and zinc and Bacillus subtilis and in the control treatment. The treatments with trifloxystrobin+tebuconazole reduced the presence of bite marks on the flowers and of pollen grains on the flower stigma. The fruits of the control treatments and treatments with B. subtilis and copper hydroxide were larger and had greater mass, as compared to other agrochemicals. Thus, a higher number of pesticide applications on the tomatoes reduced bee visitation rates to the flowers and, consequently, reduced the amount of pollen grains deposited on the stigmas, also reducing the fruit production. 

Keywords

bees, pollen load, Bacillus subtilis, Trifloxystrobin, Tebuconazole, compatibility of agrochemicals

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References

  1. Artz, D.R. and T.L. Pitts-Singer. 2015. Effects of fungicide and adjuvant sprays on nesting behavior in two managed solitary bees, Osmia lignaria and Megachile rotundata. PloS One 10, e0135688. Doi: 10.1371/journal.pone.0135688
  2. Barbosa, W.F., G. Smagghe, and R.N.C. Guedes. 2015. Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives. Pest. Manag. Sci. (8)71, 1049-1053. Doi: 10.1002/ps.4025
  3. Carvalho, S.M., G.A. Carvalho, C.F. Carvalho, J.S.S. Bueno-Filho, and A.P.M. Baptista. 2009. Toxicidade de acaricidas/inseticidas empregados na citricultura para a abelha africanizada Apis mellifera L., 1758 (Hymenoptera: Apidae). Arq. Inst. Biol. (4)76, 597-606.
  4. Costa, L.M., T.C. Grella, R.A. Barbosa, O. Malaspina, and R.C.F. Nocelli. 2015. Determination of acute lethal doses (LD50 and LC50) of imidacloprid for the native bee Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae). Sociobiology (4)62, 578-582. Doi: 10.13102/sociobiology.v62i4.792
  5. Dafni, A., E. Pacini, and M. Nepi. 2005. Pollen and stigma biology. pp 83-142. In: Dafni, A., P. Kevan, and B. Husband, (eds.). Practical pollination biology. Ontario, Canada.
  6. Degrandi-Hoffman, G., Y. Chen, E.W. Dejong, M.L. Chambers, and G. Hidalgo. 2015. Effects of oral exposure to fungicides on honey bee nutrition and virus levels. J. Econ. Entomol. (6)251, 1-11. Doi: 10.1093/jee/tov251
  7. Embrapa, 2006. Sistema brasileiro de classificação de solos. 2nd ed. Rio de Janeiro, Brazil.
  8. Fletcher, M. and L. Barnett. 2003. Bee poisoning incidents in the United Kingdom. Bull. Insectol. 56, 141-145.
  9. Franceschinelli, E.V., M.A. Elias, L.L. Bergamini, C.M. Silva-Neto, and E.R. Sujii. 2017. Influence of landscape context on the abundance of native bee pollinators in tomato crops in Central Brazil. J. Ins. Cons. 21(4), 715-726. Doi: 10.1007/s10841-017-0015-y
  10. Freitas, B.M. and J.N. Pinheiro. 2010. Efeitos sub-letais dos pesticidas agrícolas e seus impactos no manejo de polinizadores dos agroecossistemas brasileiros. Oecologia 14, 282-298. Doi: 10.4257/oeco.2010.1401.17
  11. Gill, R.J. and N.E. Raine. 2014. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Funct. Ecol. (1)28, 1459-1471. Doi: 10.1111/1365-2435.12292
  12. Hopwood, J., M. Vaughan, M. Shepherd, D. Biddinger, E. Mader, S.H. Black, and C. Mazzacano. 2012. Are neonicotinoids killing bees? A review of research into the effects of neonicotinoid insecticides on bees, with recommendations for action. Xerces Society for Intervertebrate Conservation, Portland, OR.
  13. Jacob, C.R.O., H.M. Soares, S.M. Carvalho, R.C.F. Nocelli, and O. Malaspina. 2013. Acute toxicity of fipronil to the stingless bee Scaptotrigona postica Latreille. Bull. Environ. Contam. Toxicol. (1)90, 69-72. Doi: 10.1007/s00128-012-0892-4
  14. Johnson, R.M., L. DahlGren, B.D. Siegfried, and M.D. Ellis. 2013. Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PloS One 8, e54092. Doi: 10.1371/journal.pone.0054092
  15. Lima, M.A.P., G.F. Martins, E.E. Oliveira, and R.N.C. Guedes. 2016. Agrochemical-induced stress in stingless bees: peculiarities, underlying basis, and challenges. J. Comp. Physiol. A. (9-10)202, 733-747. Doi: 10.1007/s00359-016-1110-3
  16. McFrederick, Q.S., G. Ulrich, R. Mueller, and R. James. 2014. Interactions between fungi and bacteria influence microbial community structure in the Megachile rotundata larval gut. Proc. R. Soc. Lond. B. Biol. Sci. (1779)281, 1-8.
  17. Morandin, L.A., T.M. Laverty, and P.G. Kevan. 2001a. Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses. J. Econ. Entomol. (2)94, 462-467. Doi: 10.1603/0022-0493-94.2.462
  18. Morandin, L.A., T.M. Laverty, and P.G. Kevan. 2001b. Effect of bumble bee (Hymenoptera: Apidae) pollination intensity on the quality of greenhouse tomatoes. J. Econ. Entomol. (1)94, 172-179. Doi: 10.1603/0022-0493-94.1.172
  19. Mussen, E.C.M., I. Julio, E. Lopez, and C.Y. Peng. 2004. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environ. Entomol. (5)33, 1151-1154. Doi: 10.1603/0046-225X-33.5.1151
  20. Ngugi, H.K., S. Dedej, K.S. Delaplane, A.T. Savelle, and H. Scherm. 2005. Effect of flowerapplied Serenade biofungicide (Bacillus subtilis) on pollination-related variables in rabbiteye blueberry. Biol Control (1)33, 32-38. Doi: 10.1016/j.biocontrol.2005.01.002
  21. Nunes-Silva, P., M. Hnrcir, L. Shipp, V.L. Imperatriz-Fonseca, and P.G. Kevan. 2013. The behaviour of Bombus impatiens (Apidae, Bombini) on tomato (Lycopersicon esculentum Mill., Solanaceae) flowers: pollination and reward perception. J. Pollinat. Ecol. (5)11, 33-40.
  22. Park, H.H., J.J. Kim, K.H. Kim, and S.G. Lee. 2013. Dissemination of Bacillus subtilis by using bee-vectoring technology in cherry tomato greenhouses. Korean J. Appl. Entomol. (4)52, 357-364. Doi: 10.5656/KSAE.2012.09.0.046
  23. Peel, M.C., L.F. Brian, and T.A. McMahon. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. Discuss. (2)4, 439-473. Doi: 10.5194/hessd-4-439-2007
  24. Pettis, J.S., E.M. Lichtenberg, M. Andree, J. Stitzinger, and R. Rose. 2013. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS One 8, e70182. Doi: 10.1371/journal.pone.0070182
  25. Pignati, W.A., A.N.D.S. Lima, S.S.D. Lara, M.L.M. Correa, J.R. Barbosa, L.H.D.C. Leão, and M.G. Pignatti. 2017. Spatial distribution of pesticide use in Brazil: a strategy for Health Surveillance. Cien. Saude Colet. 22(10), 3281-3293. Doi: 10.1590/1413-812320172210.17742017
  26. Riedl, H., E. Johansen, L. Brewer, and J. Barbour. 2006. How to reduce bee poisoning from pesticides. Oregon State University; University of Idaho; Washington State University, Corvallis, OR.
  27. Rocha, M.C.L.S.A. 2012. Efeitos dos agrotóxicos sobre as abelhas silvestres no Brasil: proposta metodológica de acompanhamento. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Brasilia, Brazil.
  28. Rodrigues, C.G., A.P. Kruger, W.F. Barbosa, and R.N.C. Guedes. 2016. Leaf fertilizers affect survival and behavior of the neotropical stingless bee Friesella schrottkyi (Meliponini: Apidae: Hymenoptera). J. Econ. Entomol. (30)109, 1001-1008. Doi: 10.1093/jee/tow044
  29. Sanchez-Bayo, F. and K. Goka. 2014. Pesticide residues and bees - a risk assessment. PLoS ONE 9, e94482. Doi: 10.1371/journal.pone.0094482
  30. Santos, A.B. and F.S. Nascimento. 2011. Diversidade de visitantes florais e potenciais polinizadores de Solanum lycopersicum (Linnaeus) (Solanales: Solanaceae) em cultivos orgânicos e convencionais. Neotrop. Biol. Conserv. (3)6, 162-169.
  31. Silva-Neto, C.M., F.G. Lima, B.B. Gonçalves, L.L. Bergamini, B.A. Bergamini, M.A.S. Elias, and E.V. Franceschinelli. 2013. Native bees pollinate tomato flowers and increase fruit production. J. Pollinat. Ecol. (6)11, 41-45.
  32. Silva-Neto, C.M., E.V. Franceschinelli, L.L. Bergamini, M.A.S. Elias, J.M. Morais, G.L. Moreira, B.A. and Bergamini. 2016. High species richness of native pollinators in brazilian tomato crops. Braz. J. Biol. (3)77, 506-513. Doi: 10.1590/1519-6984.17515
  33. Siqueira, K.M.N. 2008. Estudo comparativo da polinização de Mangifera indica L. em cultivo convencional e orgânico na região do Vale do Submédio do São Francisco. Rev. Bras. Fruti. 30, 303-310. Doi: 10.1590/S0100-29452008000200006
  34. Solomon, M.G. and K.J.M. Hooker. 1989. Chemical repellents for reducing pesticide hazard to honeybees in apple orchards. J. Apic. Res. (4)28, 223-227. Doi: 10.1080/00218839.1989.11101188
  35. Spadotto, C.A., M.A.F. Gomes, L.C. Luchini, and M.M. Andrea. 2004. Monitoramento de risco ambiental de agrotóxicos: princípios e recomendações. Jaguaríuna, São Paulo.
  36. Thompson, H.M. 2003. Behavioural effects of pesticides in bees - their potential for use in risk assessment. Ecotoxicol. (1-4)12, 317-330. Doi: 10.1023/A:1022575315413
  37. Tomé, H.V.V., W.F. Barbosa, A.S. Correa, L.M. Gontijo, G.F. Martins, and R.N.C Guedes. 2015. Reduced risk insecticides in Neotropical stingless bee species: impact on survival and activity. Ann. Appl. Biol. (2)167, 186-196. Doi: 10.1111/aab.12217
  38. Vale, F.X.R., C.A. Lopes, and M.A.R. Alvarenga. 2013. Doenças fúngicas, bacterianas e causadas por nematoides. pp. 275-326. In: Alvarenga, M.A.R. (eds.), Tomate. Produção em campo, casa de vegetação e hidroponia. Editora Universitária de Lavras, Lavras, Brazil.

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