Sublethal effects of neonicotinoids in bees: a review

N. C. Pereira, T. O. Diniz, M. C. C. R. Takasusuki

Resumo


Beginning in 2006, beekeepers on the east coast of the United States began to report severe declines in their honeybee colonies. Because of the severity and unusual circumstances of these declines, scientists have called this phenomenon colony collapse disorder (CCD). In 2019, 500 million dead bees were found in Brazil. Analyzes of dead bees identified agrochemicals in approximately 80% of them. Thus, it is believed that one of the main causes for CCD is the intensive use of agrochemicals. Neonicotinoids are the most widely used class of insecticides in the world, they are used for pest control in a variety of crops. However, they can not only affect insects considered pests, but also non-target organisms, such as pollinators. This class of insecticides is divided into five main active ingredients: imidacloprid, thiamethoxam, clothianidin, thiacloprid and acetamiprid. Several studies demonstrate that sublethal concentrations of these insecticides affect bees in different ways, such as navigation memory and muscle movements. Thus, this review aims to report the studies published between 2014 and 2019 regarding the contamination of bees with sublethal doses of the five active ingredients of the neonicotinoid class. Imidacloprid and thiamethoxam are the most used insecticides of this class and show high toxicity to bees. On the other hand, clothianidin showed the least sublethal effects on bees on the studies reported on this review. Thiacloprid and acetamiprid, although less used in agriculture, also impair several aspects of bee health. Thus, it is possible to infer that neonicotinoids are contributing to the disappearance of bees worldwide.


Palavras-chave


imidacloprid, thiamethoxam, clothianidin, thiacloprid, acetamiprid

Texto completo:

PDF (English)

Referências


ABBO, P.M., KAWASAKI, J.K., HAMILTON, M., COOK, S.C., DEGRANDI-HOFFMAN, G., LI, W.F., LIU J., CHEN, Y.P. Effects of Imidacloprid and Varroa destructor on survival and health of European honey bees, Apis mellifera. Insect Science. Vol. 24, p 467-477, 2017.

ABDERKADER, F.B., KAIRO, G., TCHAMITCHIAN, S., BONNET, M., COUSIN, M., BARBOUCHE, N., BELZUNCES, L.P., BRUNET, J.L. Effects of Clothianidin exposure on semen parameters of honey bee drones. Journal of New Sciences. Vol. 59, p 3791-3798, 2018.

AIZEN, M. A., GARIBALDI, L. A., CUNNINGHAM, S. A., KLEIN, A. M. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Current Biology. Vol. 18, p 1572-1575, 2008.

ANDERSON, N.L., HARMON-THREATT, A.N. Chronic contact with realistic soil concentrations of imidacloprid affects the mass, immature development speed, and adult longevity of solitary bees. Scientific Reports. Vol. 9, p 3724, 2019.

BLACQUIÈRE, T., SMAGGHE, G., VAN GESTEL, C.A.M., MOMMAERTS, V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology. Vol. 21, p 973-992, 2012.

BLANKEN, L. J., VAN LANGEVELDE, F., VAN DOOREMALEN, C. Interaction between Varroa destructor and imidacloprid reduces flight capacity of honeybees. Proceedings of the Royal Society. Vol. 282, p. 20151738, 2015.

BONMATIN, J.M., GIORIO, C., GIROLAMI, V., GOULSON, D., KREUTZWEISER, D.P., KRUPKE, C., LIESS, M., LONG, E., MARZARO, M., MITCHELL, E.A., NOOME, D.A., SIMON-DELSO, N., TAPPARO, A. Environmental fate and exposure, neonicotinoids and fipronil. Environmental Science and Pollution Research. Vol. 22, p 35-67, 2015.

BOVI, T.S., ZALUSKI, T., ORSI, R.O. Toxicity and motor changes in Africanized honey bees (Apis mellifera L.) exposed to fipronil and imidacloprid. Anais da Academia Brasileira de Ciências. Vol. 90, p 239-245, 2018.

BRANDT, A., GORENFLO, A., SIEDE, R., MEIXNER, M., BUCHLER, R. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). Journal of Insect Physiology. Vol. 86, p 40-47, 2016.

BRITTAIN, C., POTTS, S G. The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic and Applied Ecology. Vol. 12, p. 321-331, 2011.

CHRISTEN, V., SCHIRRMANN, M., FREY, J.E., FENT, K. Global Transcriptomic Effects of Environmentally Relevant Concentrations of the Neonicotinoids Clothianidin, Imidacloprid, and Thiamethoxam in the Brain of Honey Bees (Apis mellifera). Environmental Science and Technology. Vol. 52, p 7534-7544, 2018.

COSTA, L.M., GRELLA, T.C., BARBOSA, R.A., MALASPINA, O., NOCELLI, R.C.F. Determination of acute lethal doses (LD50 and LC50) of imidacloprid for the native bee Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae). Sociobiology. Vol. 62, p 578-582, 2015.

COULON, M., SCHURR, F., MARTEL, A.C., COUGOULE, N., BEGAUD, A., MANGONI, P., DALMON, A., ALAUX, C., LE CONTE, Y., THIÉRY, R., RIBIÈRE-CHABERT, M., DUBOIS, E.. Metabolisation of thiamethoxam (a neonicotinoid pesticide) and interaction with the chronic bee paralysis virus in honeybees. Pesticide Biochemistry and Physiology. Vol. 144, p 10-18, 2018.

CRESSWELL, J.E., ROBERT, F.X.L., FLORANCE, H., SMIRNOFF, N. Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Management Science. Vol. 70, p 332-337, 2014.

CUTLER, G.C., SCOTT-DUPREE, C.D., SULTAN, M., MCFARLANE, A.D., BREWER, L. A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ. Vol. 2, p e652, 2014.

DANFORTH, B.N. Bees. Current Biology. Vol. 17, p R156-R161, 2007.

DANFORTH, B.N., MINCKLEY, R.L., NEFF, J.L. The Solitary Bees – Biology, Evolution, Conservation. Princeton, Princeton University Press, 2019. 471p.

DE SMET, L., HATJINA, F., IOANNIDIS, P., HAMAMTZOGLOU, A., SCHOONVAERE, K., FRANCIS, F., MEEUS, I., SMAGGHE, G., GRAAF, D.C. Stress indicator gene expression profiles, colony dynamics and tissue development of honey bees exposed to sub-lethal doses of imidacloprid in laboratory and field experiments. PLoS ONE. Vol. 12, p e0171529, 2017.

DECOURTYE, A., DEVILLERS, J., GENECQUE, E., LE MENACH, K., BUDZINSKI, H., CLUZEAU, S., PHAM-DELEGUE, M.H. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Archives of Environmental Contamination and Toxicology. Vol. 48, p 242-250, 2005.

DELAPLANE, K.S., MAYER, D.R., MAYER, D.F. Crop Pollination by Bees. London: CABI Publishing, 2000. 352 p.

DEVAUD, J., PAPOUIN, T., CARCAUD, J., SANDOZ, J., GRÜNEWALD, B., GIURFA, M. Neural substrate for higher‐order learning in an insect: Mushroom bodies are necessary for configural discriminations. Proceedings of the National Academy of Sciences of the USA. Vol. 112, p E5854-E5862, 2015.

DIAO, Q., LI, B., ZHAO, H., WU, Y., GUO, R., DAI, P., CHEN, D., WANG, Q., HOU, C. Enhancement of chronic bee paralysis virus levels in honeybees acute exposed to imidacloprid: A Chinese case study. Science of the Total Environment. Vol. 630, p 487-494, 2018.

DIETZSCH, A.C., KUNZ, N., WIRTZ, I.P., STAHLER, M., HEIMBACH, U., PISTORIUS, J. Does winter oilseed rape grown from clothianidin-coated seeds affect experimental populations of mason bees and bumblebees? A semi-field and field study. Journal of Consumer Protection and Food Safety. Vol. 1, p 1-16, 2019.

DIVELY, G.P., EMBREY, M.S., KAMEL, A., HAWTHORNE, D.J., PETTIS, J.S. Assessment of Chronic Sublethal Effects of Imidacloprid on Honey Bee Colony Health. PLoS ONE. Vol. 10, p e0126043, 2015.

ELBERT, A., HAAS, M., SPRINGER, B., THIELERT, W., NAUEN, R. Applied aspects of neonicotinoid uses in crop protection. Pest Management Science. Vol. 64, p 1099-1105, 2008.

ELLIS, C., PARK, K.J., WHITEHORN, P., DAVID, A., GOULSON, D. The Neonicotinoid Insecticide Thiacloprid Impacts upon Bumblebee Colony Development under Field Conditions. Environmental Science & Technology. Vol. 51, p 1727-1732, 2017.

EUROPEAN FOOD SAFETY AUTHORITY. Peer review of the pesticide risk assessment for the active substance imidacloprid in light of confirmatory data submitted. European Food Safety Authority Journal. Vol. 14, p e04607, 2016.

FAHRBACH, S.E., VAN NEST, B.N. Synapsin-based approaches to brain plasticity in adult social insects. Current Opinion in Insect Science. Vol. 18, p 27-34, 2016.

FORFERT, N., MORITZ, R.F.A. Thiacloprid alters social interactions among honey bee workers (Apis mellifera). Journal of Apicultural Research. Vol. 56, p 467-474, 2017.

FRAZIER, M., MULLIN, C., FRAZIER, J., ASHCRAFT, S. What have pesticides got to do with it? American Bee Journal. Vol. 148, p 521-523, 2008.

FRIOL, P.S., CATAE, A.F., TAVARES, D.A., MALASPINA, O., ROAT, T.C. Can the exposure of Apis mellifera (Hymenoptera, Apidae) larvae to field concentration of thiamethoxam affect newly emerged bees? Chemosphere. Vol. 185, p 56-66, 2017.

GAJGER, I.T., SAKAC, M., GREGORC, A. Impact of Thiamethoxam on Honey Bee Queen (Apis mellifera carnica) Reproductive Morphology and Physiology. Bulletin of Environmental Contamination and Toxicology. Vol. 99, p 297-302, 2017.

GAUTHIER, M., ARAS, P., PAQUIN, J., BOILY, M. Chronic exposure to imidacloprid or thiamethoxam neonicotinoid causes oxidative damages and alters carotenoid-retinoid levels in caged honey bees (Apis mellifera). Scientific Reports. Vol, 8, p 16274, 2018.

GODFRAY, H.C.J., BLACQUIÈRE, T., FIEDL, L.M., HAILS, R.S., POTTS, S.G., RAINE, N.E., VANGERGEN, A.J., MCLEAN, A.R. A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences. Vol. 282, p 20151821, 2015.

GOULSON, D., NICHOLLS, E., BOTIAS, C., ROTHERAY, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. Vol. 347, p 1255957, 2015.

GREGORC, A., ELLIS, J.D. Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pesticide Biochemistry and Physiology. Vol. 99, p 200-207, 2011.

HAVSTADA, L.T., ØVERLANDB, J.I., VALAND, S., AAMLID, T.S. Repellency of insecticides and the effect of thiacloprid on bumblebee colony development in red clover (Trifolium pratense L.) seed crops. Acta Agriculturae Scandinavica, Section B — Soil & Plant Science. Vol. 69, p 439-451, 2019.

HENRY, M., BÉGUIN, M., REQUIER, F., ROLLIN, O., ODOUX, J.-F., AUPINEL, P., APTEL, J., TCHAMITCHIAN, S., DECOURTYE, A. A common pesticide decreases foraging success and survival in honey bees. Science. Vol. 336, p 348-350, 2012.

IQBAL, J., ALQARNI, A.S., RAWEH, H.S.A. Effect of Sub-lethal Doses of Imidacloprid on Learning and Memory Formation of Indigenous Arabian Bee (Apis mellifera jemenitica Ruttner) Adult Foragers. Neotropical Entomology. Vol. 48, p 373-380, 2019.

JESCHKE, P., NAUEN, R., SCHINDLER, M., ELBERT, A. Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry Vol. 59, p 2897-2908, 2011.

JIN, N., KLEIN, S., LEIMIG, F., BISCHOFF, G., MENZEL, R. The neonicotinoid clothianidin interferes with navigation of the solitary bee Osmia cornuta in a laboratory test. Journal of Experimental Biology. Vol. 218, p 2821-2825, 2015.

JOHNSON, R. Honey Bee Colony Collapse Disorder. Disponível em: https://cursa.ihmc.us/rid=1JJM69DXL-27XB9CC-12CF/bees.pdf

KARAHAN, A., ÇAKMAK, I., HRANITZ, J.M., KARACA, I., WELLS, H. Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology. Vol. 24, p 2017-2025, 2015.

LANOT, R., ZACHARY, D., HOLDER, F., MEISTER, M. Postembryonic hematopoiesis in Drosophila. Developmental Biology. Vol. 230, p 243-257, 2001.

LU, C., WARCHOL, K.M., CALLAHAN, R.A. Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bulletin of Insectology. Vol, 67, p 125-130, 2014.

LUNARDI, J.S., ZALUSKI, R., ORSI, R.O. Evaluation of Motor Changes and Toxicity of Insecticides Fipronil and Imidacloprid in Africanized Honey Bees (Hymenoptera: Apidae). Sociobiology. Vol. 64, p 50-56, 2017.

MEIKLE, W.G., ADAMCZYK, J.J., WEISS, M., GREGORC, A., JOHNSON, D.R., STEWART, S.D., ZAWISLAK, J., CARROLL, M.J., LORENZ, G.M. Sublethal Effects of Imidacloprid on Honey Bee Colony Growth and Activity at Three Sites in the U.S. PLoS ONE. Vol. 11, p e0168603, 2016.

MOREIRA, A.A.G., LIMA-NETO, P., CAETANO, E.W.S., BARROSO-NETO, I.L., FREIRE, V.N. The vibrational properties of the bee-killer imidacloprid insecticide: A molecular description. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy. Vol. 185, p 245-255, 2017.

MOREIRA, D.R., GIGLIOLLI, A.A.S., FALCO, J.R.P., JULIO, A.H.F., VOLNISTEM, E.A., CHAGAS, F., TOLEDO, V.A.A., RUVOLO-TAKASUSUKI, M.C.C. Toxicity and effects of the neonicotinoid thiamethoxam on Scaptotrigona bipunctata lepeletier, 1836 (Hymenoptera: Apidae). Toxicology. Vol. 33, p 463-475,2018.

MORFIN, N., GOODWIN, P.H., HUNT, G.J., GUZMAN-NOVOA, E. Effects of sublethal doses of clothianidin and/or V. destructor on honey bee (Apis mellifera) selfgrooming behavior and associated gene expression. Scientific Reports. Vol. 9, p 5196, 2019.

NAHAR, N., OHTANI, T. Imidacloprid and Fipronil induced abnormal behavior and disturbed homing of forager honey bees Apis mellifera. Journal of Entomology and Zoology Studies. Vol. 3, p 65-72, 2015.

NICHOLLS, E., FOWLER, R., NIVEN, J.E., GILBERT, J.D., GOULSON, D. Larval exposure to field-realistic concentrations of clothianidin has no effect on development rate, over-winter survival or adult metabolic rate in a solitary bee, Osmia bicornis. PeerJ. Vol. 5, p e3417, 2017.

ODEMER, R., NILLES, L., LINDER, N., ROSENKRANZ, P. Sublethal effects of clothianidin and Nosema spp. on the longevity and foraging activity of free flying honey bees. Ecotoxicology. Vol. 27, p 527-538, 2018.

OMIROU, M., VRYZAS, Z., PAPADOPOULOU-MOURKIDOUB, E., ECONOMOUA, A. Dissipation rates of iprodione and thiacloprid during tomato production in greenhouse. Food Chemistry. Vol. 116, p 499-504, 2009.

PENG, Y.C., YANG, E.C. Sublethal dosage of imidacloprid reduces the microglomerular density of honey bee mushroom bodies. Scientific Reports. Vol. 6, p 19298, 2016.

RAND, E.E., SMIT, S., BEUKES, M., APOSTOLIDES, Z., PIRK, C.W., NICOLSON, S.W. Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Scientific Reports. Vol. 5, p 11779, 2015.

RAVAIANO, S.V., BARBOSA, W.F., TOMÉ, H.V.V., CAMPOS, L.A.O., MARTINS, G.F. Acute and oral exposure to imidacloprid does not affect the number of circulating hemocytes in the stingless bee Melipona quadrifasciata post immune challenge. Pesticide Biochemistry and Physiology. Vol. 152, p 24-28, 2018.

SÁNCHEZ-BAYO, F., BELZUNCES, L., BONMATIN, J.M. Lethal and sublethal effects, and incomplete clearance of ingested imidacloprid in honey bees (Apis mellifera). Ecotoxicology. Vol. 26, p 1199-1206, 2017.

SATYAVATHI, V.V., MINZ, A., NAGARAJU, J. Nodulation: An unexplored cellular defense mechanism in insects. Cellular Signalling. Vol. 26, p. 1753-1763, 2014.

SHI, T., BURTON, S., WANG, Y., XU, S., ZHANG, W., YU, L. Metabolomic analysis of honey bee, Apis mellifera L. response to thiacloprid. Pesticide Biochemistry and Physiology. Vol. 152, p 17-23, 2018.

SHI, T.F., WANG, Y.F., LIU, F., QI, L., YU, L.S. Influence of the Neonicotinoid Insecticide Thiamethoxam on miRNA Expression in the Honey Bee (Hymenoptera: Apidae). Journal of Insect Science. Vol. 17, p 1-5, 2017a.

SHI, T.F., WANG, Y.F., LIU, F., QI, L., YU, L.S. Sublethal Effects of the Neonicotinoid Insecticide Thiamethoxam on the Transcriptome of the Honey Bees (Hymenoptera: Apidae). Journal of Economic Entomology. Vol. XX, p 1-7, 2017b.

SIEDE, R., FAUST, L., MEIXNER, M.D., MAUS, C., GRUNEWALD, B., BUCHLER, R. Performance of honey bee colonies under a long-lasting dietary exposure to sublethal concentrations of the neonicotinoid insecticide thiacloprid. Pest Management Science. Vol. 73, p 1334-1344, 2017.

SIEDE, R., MEIXNER, M.D., ALMANZA, M.T., SCHONING, R., MAUS, C., BUCHLER, R. A long-term field study on the effects of dietary exposure of clothianidin to varroosis-weakened honey bee colonies. Ecotoxicology. Vol. 27, p 772-783, 2018.

SIMON-DELSO, N., AMARAL-ROGERS, V., BELZUNCES, L.P. et al. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environmental Science and Pollution Research. Vol. 22, p 5-34, 2014.

SOARES, H.M., JACOB, C.R.O., CARVALHO, S.M., NOCELLI, R.C.F., MALASPINA, O. Toxicity of Imidacloprid to the Stingless Bee Scaptotrigona postica Latreille, 1807 (Hymenoptera: Apidae). Bulletin of Environmental Contamination and Toxicology. Vol. 94, p 675-680, 2015.

STERK, G., PETERS, B., GAO, Z., ZUMKIER, Y. Large-scale monitoring of effects of clothianidin-dressed OSR seeds on pollinating insects in Northern Germany: effects on large earth bumble bees (Bombus terrestris). Ecotoxicology. Vol. 25, p 1666-1678, 2016.

STONER, K.A., EITZER, B.D. Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One. Vol. 7, p e39114, 2012.

TAVARES, D.A., ROAT, T.C., CARVALHO, S.M., SILVA-ZACARIN, E.C.M., MALASPINA, O. In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere. Vol. 135, p 370-378, 2015.

TAVARES, D.A., ROAT, T.C., SILVA-ZAVARIN, E.C.M., NOCELLI, R.C.F., MASPINA, O. Exposure to thiamethoxam during the larval phase affects synapsin levels in the brain of the honey bee. Ecotoxicology and Environmental Safety. Vol. 169, p 523-528, 2019.

TELANGRE, A.H., MATRE, Y.B., LATPATE, C.B., ZANWAR, P.R. Effect of neonicotinoids i.e acetamiprid 20% SP on foraging behaviour of honey bee on safflower (Carthamus tinctorius L.). International Journal of Chemical Studies. Vol. 6, p 185-188, 2018.

THANY, S.H., BOURDIN, C.M., GRATON, J., LAURENT, A.D., MATHÉ-ALLAINMAT, M., LEBRETON, J., QUESTEL, J.Y.L. Similar Comparative Low and High Doses of Deltamethrin and Acetamiprid Differently Impair the Retrieval of the Proboscis Extension Reflex in the Forager Honey Bee (Apis mellifera). Insects. Vol. 6, p 805-814, 2015.

TISON, L., HAHN, M.L., HOLTZ, S., RÖßNER, A., GREGGERS, U., BISCHOFF, G., MENZEL, R. Honey Bees’ Behavior Is Impaired by Chronic Exposure to the Neonicotinoid Thiacloprid in the Field. Environmental Science & Technology. Vol. 50, p 7218-7227, 2016.

TISON, L., HOLTZ, S., ADEOYE, A., KALKAN, O., IRMISCH, N.S., LENMANN, N., MENZEL, R. Effects of sublethal doses of thiacloprid and its formulation Calypso® on the learning and memory performance of honey bees. Journal of Experimental Biology. Vol. 220, p 3695-3705, 2017.

TISON, L., RÖßNER, A., GERSCHEWSKI, S., MENZEL, R. The neonicotinoid clothianidin impairs memory processing in honey bees. Ecotoxicology and Environmental Safety. Vol. 180, p 139-145, 2019.

TOSI, S., BURGIO, G., NIEH, J.C. A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Scientific Reports. Vol. 7, p 1201, 2017.

TOSI, S., NIEH, J.C. A common neonicotinoid pesticide, thiamethoxam, alters honey bee activity, motor functions, and movement to light. Scientific Reports. Vol. 7, p 15132, 2017.

VAN DOOREMALEN, C., CORNELISSEN, B., POLEIJ-HOK-AHIN, C., BLACQUIÈRE, T. Single and interactive effects of Varroa destructor, Nosema spp., and imidacloprid on honey bee colonies (Apis mellifera). Ecosphere. Vol. 9, p e02378, 2018.

WILLIAMS, D. The Case of the Missing Bees. Penn State Agriculture, Winter/Spring:18-25, 2008.

WU, M.C., CHANG, Y.W., LU, K.H., YANG, E.C. Gene expression changes in honey bees induced by sublethal imidacloprid exposure during the larval stage. Insect Biochemistry and Molecular Biology. Vol. 88, p 12-20, 2017a.

WU, Y.Y, ZHOU, T., WANG, Q., DAI, P.L., XU, S.F., JIA, H.R., WANG, X. Programmed Cell Death in the Honey Bee (Apis mellifera) (Hymenoptera: Apidae) Worker Brain Induced by Imidacloprid. Journal of Economic Entomology. Vol. 108, p 1486-1494, 2015.

WU, Y.Y., LUO, Q.H., HOU, C.S., WANG, Q., DAI, P.L., GAO, J., LIU, Y.J., DIAO, Q.Y. Sublethal effects of imidacloprid on targeting muscle and ribosomal protein related genes in the honey bee Apis mellifera L. Scientific Reports. Vol. 7, p 15943, 2017b.

YAO, J., ZHU, Y.C., ADAMCZYK, J. Responses of Honey Bees to Lethal and Sublethal Doses of Formulated Clothianidin Alone and Mixtures. Journal of Economic Entomology. Vol. 111, p 1517-1525, 2018.

YAO, X.H., MIN, H., LU, Z.H., YUAN, H.P. Influence of acetamiprid on soil enzymatic activities and respiration. European Journal of Soil Biology. Vol. 42, p 120-126, 2006.

ZHANG, E., NIEH, J.C. The neonicotinoid imidacloprid impairs honey bee aversive learning of simulated predation. Journal of Experimental Biology. Vol. 218, p 3199-3205, 2015.




DOI: http://dx.doi.org/10.36560/13720201120

Apontamentos

  • Não há apontamentos.


Apoio:
Endereço: 
Universidade Federal de Rondonópolis
Avenida dos Estudantes, 5055 - Cidade Universitária
Rondonópolis - MT, 78735-901