Interaction between biological and chemistry fungicides and tomato pollinators

Interacción entre fungicidas biológicos y químicos con polinizadores de tomate

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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


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. 



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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

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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