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Abstract:

Glyphosate (GLY) is a broad-spectrum herbicide used for weed control. The sub-lethal impact of GLY on non-target organisms such as insect pollinators has not yet been evaluated. Apis mellifera is the main pollinator in agricultural environments and is a well-known model for behavioural research. Honeybees are also accurate biosensors of environmental pollutants and their appetitive behavioural response is a suitable tool with which to test sub-lethal effects of agrochemicals. We studied the effects of field-realistic doses of GLY on honeybees exposed chronically or acutely to the herbicide. We focused on sucrose sensitivity, elemental and non-elemental associative olfactory conditioning of the proboscis extension response (PER), and foraging-related behaviour. We found a reduced sensitivity to sucrose and learning performance for the groups chronically exposed to GLY concentrations within the range of recommended doses. When olfactory PER conditioning was performed with sucrose reward with the same GLY concentrations (acute exposure), elemental learning and short-term memory retention decreased significantly compared with controls. Non-elemental associative learning was also impaired by an acute exposure to GLY traces. Altogether, these results imply that GLY at concentrations found in agro-ecosystems as a result of standard spraying can reduce sensitivity to nectar reward and impair associative learning in honeybees. However, no effect on foragingrelated behaviour was found. Therefore, we speculate that successful forager bees could become a source of constant inflow of nectar with GLY traces that could then be distributed among nestmates, stored in the hive and have long-term negative consequences on colony performance. © 2014. Published by The Company of Biologists Ltd

Registro:

Documento: Artículo
Título:Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour
Autor:Herbert, L.T.; Vázquez, D.E.; Arenas, A.; Farina, W.M.
Filiación:Departamento de Biodiversidad y Biología Experimental, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, C1428EHA, Argentina
Palabras clave:Apis mellifera; Associative learning; Glyphosate; Sensitivity to reward; Sub-lethal effects; glycine; glyphosate; herbicide; sucrose; analogs and derivatives; animal; appetite; bee; conditioned reflex; drug effects; learning; odor; physiology; reward; short term memory; Animals; Appetitive Behavior; Association Learning; Bees; Conditioning, Classical; Glycine; Herbicides; Memory, Short-Term; Reward; Smell; Sucrose
Año:2014
Volumen:217
Número:19
Página de inicio:3457
Página de fin:3464
DOI: http://dx.doi.org/10.1242/jeb.109520
Título revista:Journal of Experimental Biology
Título revista abreviado:J. Exp. Biol.
ISSN:00220949
CODEN:JEBIA
CAS:glycine, 56-40-6, 6000-43-7, 6000-44-8; glyphosate, 1071-83-6; sucrose, 122880-25-5, 57-50-1; Glycine; glyphosate; Herbicides; Sucrose
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00220949_v217_n19_p3457_Herbert

Referencias:

  • Aizen, M.A., Garibaldi, L.A., Dondo, M., Expansión de la soja y diversidad de la agricultura Argentina (2009) Ecol. Austral, 19, pp. 45-54
  • Amrhein, N., Deus, B., Gehrke, P., Steinrücken, H.C., The site of the inhibition of the shikimate pathway by glyphosate. II. Interference of glyphosate with chorismate formation in vivo and in vitro (1980) Plant Physiol., 66, pp. 830-834
  • Arenas, A., Farina, W.M., Age and rearing environment interact in the retention of early olfactory memories in honeybees (2008) J. Comp. Physiol. A, 194, pp. 629-640
  • Arenas, A., Fernández, V.M., Farina, W.M., Associative learning during early adulthood enhances later memory retention in honeybees (2009) Plos ONE, 4
  • Arenas, A., Giurfa, M., Farina, W.M., Sandoz, J.C., Early olfactory experience modifies neural activity in the antennal lobe of a social insect at the adult stage (2009) Eur. J. Neurosci., 30, pp. 1498-1508
  • Arenas, A., Giurfa, M., Sandoz, J.C., Hourcade, B., Devaud, J.M., Farina, W.M., Early olfactory experience induces structural changes in the primary olfactory center of an insect brain (2012) Eur. J. Neurosci., 35, pp. 682-690
  • Balbuena, M.S., Arenas, A., Farina, W.M., Floral scents learned inside the honeybee hive have a long-lasting effect on recruitment (2012) Anim. Behav., 84, pp. 77-83
  • Balbuena, M., Molinas, J., Farina, W., Honey bee recruitment to scented food sources: Correlations between in-hive social interactions and foraging decisions (2012) Behav. Ecol. Sociobiol., 66, pp. 445-452
  • Bitterman, M.E., Menzel, R., Fietz, A., Schäfer, S., Classical conditioning of proboscis extension in honeybees (Apis mellifera) (1983) J. Comp. Psychol., 97, pp. 107-119
  • Bohan, D.A., Boffey, C.W., Brooks, D.R., Clark, S.J., Dewar, A.M., Firbank, L.G., Haughton, A.J., May, M.J., Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape (2005) Proc. Biol. Sci., 272, pp. 463-474
  • Carlisle, S.M., Trevors, J.T., Glyphosate in the environment (1988) Water Air Soil Pollut., 39, pp. 409-420
  • Deisig, N., Lachnit, H., Giurfa, M., Hellstern, F., Configural olfactory learning in honeybees: Negative and positive patterning discrimination (2001) Learn. Mem., 8, pp. 70-78
  • Devillers, J., Pham-Delègue, M.H., (2002) Honey Bees: Estimating the Environmental Impact of Chemicals, , London; New York, NY: Taylor & Francis
  • Duke, S.O., Lydon, J., Paul, R.N., Principles of weed science (1989) Weed Science, 37, p. 152
  • Eiri, D.M., Nieh, J.C., A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing (2012) J. Exp. Biol., 215, pp. 2022-2029
  • Feng, J.C., Thompson, D.G., Reynolds, P.E., Fate of glyphosate in a Canadian forest watershed. 1. Aquatic residues and off-target deposit assessment (1990) J. Agric. Food Chem., 38, pp. 1110-1118
  • Fischer, J., Müller, T., Spatz, A.K., Greggers, U., Grünewald, B., Menzel, R., Neonicotinoids interfere with specific components of navigation in honeybees (2014) Plos ONE, 9
  • Giesy, J.P., Dobson, S., Solomon, K.R., Ecotoxicological risk assessment for roundup® herbicide (2000) Rev. Environ. Contam. Toxicol., 167, pp. 35-120
  • Giurfa, M., Cognitive neuroethology: Dissecting non-elemental learning in a honeybee brain (2003) Curr. Opin. Neurobiol., 13, pp. 726-735
  • Giurfa, M., Behavioral and neural analysis of associative learning in the honeybee: A taste from the magic well (2007) J. Comp. Physiol. A, 193, pp. 801-824
  • Goldsborough, L.G., Brown, D.J., Effect of glyphosate (Roundup formulation) on periphytic algal photosynthesis (1988) Bull. Environ. Contam. Toxicol., 41, pp. 253-260
  • Goyret, J., Farina, W.M., Non-random nectar unloading interactions between foragers and their receivers in the honeybee hive (2005) Naturwissenschaften, 92, pp. 440-443
  • Grüter, C., Farina, W.M., The honeybee waggle dance: Can we follow the steps? (2009) Trends Ecol. Evol., 24, pp. 242-247
  • Grüter, C., Farina, W.M., Past experiences affect interaction patterns among foragers and hive-mates in honeybees (2009) Ethology, 115, pp. 790-797
  • Grüter, C., Acosta, L.E., Farina, W.M., Propagation of olfactory information within the honeybee hive (2006) Behav. Ecol. Sociobiol., 60, pp. 707-715
  • Howe, C.M., Berrill, M., Pauli, B.D., Helbing, C.C., Werry, K., Veldhoen, N., Toxicity of glyphosate-based pesticides to four North American frog species (2004) Environ. Toxicol. Chem., 23, pp. 1928-1938
  • Kirchner, W.H., Mad-bee-disease? Sublethal effects of imidacloprid ('Gaucho') on the behavior of honey-bees (1999) Apidologie (Celle), 30, p. 422
  • Kirchner, W.H., Lindauer, M., Michelsen, A., Honeybee dance communication: Acoustical indications of direction in round dances (1988) Naturwissenschaften, 75, pp. 629-630
  • Kuwabara, M., Building the conditioned reflex of the Pavlov-type in the honeybee, Apis mellifera (1957) J. Fac. Sci. Hokkaido Univ. Zool., 13, pp. 458-464
  • Lunney, G.H., Using analysis of variance with a dichotomous dependent variable: An empirical study (1970) Journal of Educational Measurement, 7, pp. 263-269
  • Matsumoto, Y., Menzel, R., Sandoz, J.-C., Giurfa, M., Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: A step toward standardized procedures (2012) J. Neurosci. Methods, 211, pp. 159-167
  • Menzel, R., Memory dynamics in the honeybee (1999) J. Comp. Physiol. A, 185, pp. 323-340
  • Nixon, H.L., Ribbands, C.R., Food transmission within the honeybee community (1952) Proc. R. Soc. B, 140, pp. 43-50
  • Page, R.E., Jr., Erber, J., Levels of behavioral organization and the evolution of division of labor (2002) Naturwissenschaften, 89, pp. 91-106
  • Page, R.E., Jr., Erber, J., Fondrk, M.K., The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.) (1998) J. Comp. Physiol. A, 182, pp. 489-500
  • Relyea, R.A., The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities (2005) Ecol. Appl., 15, pp. 618-627
  • Relyea, R.A., The lethal impacts of roundup and predatory stress on six species of North American tadpoles (2005) Arch. Environ. Contam. Toxicol., 48, pp. 351-357
  • Riley, J.R., Greggers, U., Smith, A.D., Reynolds, D.R., Menzel, R., The flight paths of honeybees recruited by the waggle dance (2005) Nature, 435, pp. 205-207
  • Rueppell, O., Christine, S., Mulcrone, C., Groves, L., Aging without functional senescence in honey bee workers (2007) Curr. Biol., 17, pp. R274-R275
  • Scheiner, R., Erber, J., Page, R.E., Jr., Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.) (1999) J. Comp. Physiol. A, 185, pp. 1-10
  • Sokal, R.R., Rohlf, F.J., (1995) Biometry: The Principles and Practice of Statistics in Biological Research, , New York, NY: W. H. Freeman
  • Springett, J.A., Gray, R.A.J., Effect of repeated low doses of biocides on the earthworm Apporectodea caliginosa in laboratory culture (1992) Soil Biology and Biochemistry, 24, pp. 1739-1744
  • Takeda, K., Classical conditioned response in the honey bee (1961) J. Insect Physiol., 6, pp. 168-179
  • Tate, T.M., Spurlock, J.O., Christian, F.A., Effect of glyphosate on the development of Pseudosuccinea columella snails (1997) Arch. Environ. Contam. Toxicol., 33, pp. 286-289
  • Thom, C., Gilley, D.C., Hooper, J., Esch, H.E., The scent of the waggle dance (2007) Plos Biol., 5, p. e228
  • Thompson, H.M., Levine, S.L., Doering, J., Norman, S., Manson, P., Sutton, P., Von Mérey, G., Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example (2014) Integr. Environ. Assess. Manag., 10, pp. 463-470
  • Von Frisch, K., (1967) The Dance Language and Orientation of Bees, , Cambridge, MA: Harvard University Press
  • Von Frisch, K., Lindauer, M., Über die fluggeschwindigkeit der bienen und über ihre richtungsweisung bei seitenwind (1955) Naturwissenschaften, 42, pp. 377-385
  • Williamson, S.M., Wright, G.A., Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees (2013) J. Exp. Biol., 216, pp. 1799-1807
  • Winston, M.L., (1987) Biology of the Honey Bee, , Cambridge, MA: Harvard University Press
  • Zar, J., (1999) Biostatistical Analysis, , 4th edn. Upper Saddle River, NJ: Prentice Hall
  • Zhang, W., Jiang, F., Ou, J., Global pesticide consumption and pollution: With China as a focus (2011) Proc. Int. Acad. Ecol. Environ. Sci., 1, pp. 125-144

Citas:

---------- APA ----------
Herbert, L.T., Vázquez, D.E., Arenas, A. & Farina, W.M. (2014) . Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. Journal of Experimental Biology, 217(19), 3457-3464.
http://dx.doi.org/10.1242/jeb.109520
---------- CHICAGO ----------
Herbert, L.T., Vázquez, D.E., Arenas, A., Farina, W.M. "Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour" . Journal of Experimental Biology 217, no. 19 (2014) : 3457-3464.
http://dx.doi.org/10.1242/jeb.109520
---------- MLA ----------
Herbert, L.T., Vázquez, D.E., Arenas, A., Farina, W.M. "Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour" . Journal of Experimental Biology, vol. 217, no. 19, 2014, pp. 3457-3464.
http://dx.doi.org/10.1242/jeb.109520
---------- VANCOUVER ----------
Herbert, L.T., Vázquez, D.E., Arenas, A., Farina, W.M. Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. J. Exp. Biol. 2014;217(19):3457-3464.
http://dx.doi.org/10.1242/jeb.109520