Interacción entre fungicidas biológicos y químicos con polinizadores de tomate
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Sección: SECCION DE HORTALIZAS
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Silva-Neto, C., Ribeiro, A. C., Gomes, F., Neves, J., Melo, A., Calil, F., Nascimento, A., & Franceschinelli, E. (2018). Interacción entre fungicidas biológicos y químicos con polinizadores de tomate. Revista Colombiana De Ciencias Hortícolas, 12(2), 425-435. https://doi.org/10.17584/rcch.2018v12i2.7690
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Autores
Carlos de Melo e Silva-Neto
http://orcid.org/0000-0001-8624-3836
Anna Clara Chaves Ribeiro
http://orcid.org/0000-0002-0335-0407
Flaviana Lima Gomes
http://orcid.org/0000-0003-2824-0180
Jordana Guimarães Neves
http://orcid.org/0000-0001-8102-3236
Aniela Pilar Campos de Melo
https://orcid.org/0000-0002-5687-5928
Francine Neves Calil
https://orcid.org/0000-0003-2882-9622
Abadia dos Reis Nascimento
https://orcid.org/0000-0003-3952-5878
Edivani Villaron Franceschinelli
https://orcid.org/0000-0001-9050-8577
Resumen
El uso inapropiado de agroquímicos es perjudicial para las abejas que visitan los cultivos agrícolas, lo que reduce la producción por la afectación de la polinización y son pocos los estudios sobre este tema. El objetivo de este estudio fue verificar la incidencia de diferentes fungicidas sobre la visita de abejas en cultivos de tomate y sus efectos sobre la deposición de granos de polen en el estigma, número de semillas, masa y tamaño del fruto. Los experimentos consistieron en 10 tratamientos que fueron: (T1) tratamiento control sin agroquimicos; (T2 y T3) Bacillus subtilis en diferentes frecuencias de aplicación; (T4) hidróxido de cobre; (T5) B. subtilis e hidróxido de cobre; (T6) acibenzolar- S-metilo; (T7) trifloxistrobina+tebuconazol y B. subtilis; (T8) hidróxido de cobre + Mancozeb; (T9) propineb+(- trifloxistrobina+tebuconazol); (T10) (trifloxistrobina+tebuconazol)+B. subtilis+hidróxido de cobre. Se determinó la presencia de la marca de polinización en la flor, la carga de polen en los estigmas, el número de semillas por fruto, y el tamaño y masa de los frutos en cada tratamiento. Posteriormente, se estimó la tasa de mortalidad de Melipona quadrifasciata expuesta a cuatro fungicidas (trifloxistrobina+tebuconazol, manganeso y zinc, hidróxido de cobre, Bacillus subtilis). La tasa de mortalidad de M. quadrifasciata en 24 horas de evaluación fue mayor en los tratamientos con hidróxido de cobre y trifloxistrobina+tebuconazol (75 y 50%, respectivamente). La tasa de mortalidad fue menor en los tratamientos con manganeso y zinc, Bacillus subtilis y el tratamiento de control. Los tratamientos con trifloxistrobina y tebuconazol redujeron la presencia de marcas de mordida y granos de polen en el estigma de las flores. Los frutos de los tratamientos control y con B. subtilis e hidróxido de cobre fueron más grandes y tuvieron mayor masa. Por lo tanto, un mayor número de aplicaciones de pesticidas en las plantas de tomate reducen las tasas de visitas de abejas en las flores y en consecuencia, la cantidad de granos de polen depositados en los estigmas afectando también la producción de los frutos.
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This work is licensed under a Atribución-NoComercial-CompartirIgual 4.0 Internacional (CC BY-NC-SA 4.0)
Referencias
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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.
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
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.
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
Embrapa, 2006. Sistema brasileiro de classificação de solos. 2nd ed. Rio de Janeiro, Brazil.
Fletcher, M. and L. Barnett. 2003. Bee poisoning incidents in the United Kingdom. Bull. Insectol. 56, 141-145.
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
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
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
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.
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
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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
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.
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
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
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
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
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.
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
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
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
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
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.
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.
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
Sanchez-Bayo, F. and K. Goka. 2014. Pesticide residues and bees - a risk assessment. PLoS ONE 9, e94482. Doi: 10.1371/journal.pone.0094482
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.
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.
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
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
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
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.
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
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
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.
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
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.
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
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.
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
Embrapa, 2006. Sistema brasileiro de classificação de solos. 2nd ed. Rio de Janeiro, Brazil.
Fletcher, M. and L. Barnett. 2003. Bee poisoning incidents in the United Kingdom. Bull. Insectol. 56, 141-145.
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
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
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
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.
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
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
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
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.
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
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
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
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
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.
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
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
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
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
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.
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.
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
Sanchez-Bayo, F. and K. Goka. 2014. Pesticide residues and bees - a risk assessment. PLoS ONE 9, e94482. Doi: 10.1371/journal.pone.0094482
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.
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.
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
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
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
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.
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
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
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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