Effects of Sublethal Concentrations of Chlorpyrifos on Olfactory Learning and Memory Performances in Two Bee Species, Apis mellifera and Apis cerana

Authors

  • Zhiguo Li
  • Meng Li
  • Jingnan Huang
  • Changsheng Ma
  • Linchen Xiao
  • Qiang Huang
  • Yazhou Zhao
  • Hongyi Nie
  • Songkun Su

DOI:

https://doi.org/10.13102/sociobiology.v64i2.1385

Abstract

Chlorpyrifos is a widely used organophosphorus insecticide. The acute oral 24 h median lethal dose (LD50) value of chlorpyrifos in Apis mellifera and in Apis cerana was estimated to assess differential acute chlorpyrifos toxicity in the two bee species. The LD50 values of chlorpyrifos in A. mellifera and in A. cerana are 103.4 ng/bee and 81.8 ng/bee, respectively, which suggests A. cerana bees are slightly more sensitive than A. mellifera bees to the toxicity of chlorpyrifos. Doses half the acute LD50 of chlorpyrifos were selected to study behavioral changes in the two bee species using proboscis extension response assay. A. mellifera foragers treated with chlorpyrifos showed significantly lower response to the 10% sucrose solution compared to control bees after 2, 24 and 48 h. Chlorpyrifos significantly impaired the olfactory learning abilities and 2 h memory retention of forager bees regardless of honey bee species, which may affect the foraging success of bees exposed to chlorpyrifos.

Downloads

Download data is not yet available.

References

Chauzat, M.P., Faucon, J.P., Martel, A.C., Lachaize, J., Cougoule, N. & Aubert, M. (2006). A Survey of Pesticide Residues in Pollen Loads Collected by Honey Bees in France. Journal of Economic Entomology, 99: 253-262. doi: 10.1093/ jee/99.2.253

Decourtye, A., Armengaud, C., Renou, M., Devillers, J., Cluzeau, S., Gauthier, M. & Pham-Delègue, M.-H. (2004). Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pesticide Biochemistry and Physiology, 78: 83-92. doi: 10.1016/j.pestbp.2003.10.001

Decourtye, A., Lacassie, E. & Pham‐Delègue, M.H. (2003). Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Management Science, 59: 269-278. doi: 10.1002/ps.631

DeGrandi-Hoffman, G., Chen, Y. & Simonds, R. (2013). The effects of pesticides on queen rearing and virus titers in honey bees (Apis mellifera L.). Insects, 4: 71-89. doi: 10.3390/ insects4010071

Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., Gargiulo, G. & Pennacchio, F. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences, USA110: 18466-18471. doi: 10.1073/pnas.1314923110

Dimitrie, D.A. & Sparling, D.W. (2014). Joint toxicity of chlorpyrifos and endosulfan to Pacific treefrog (Pseudacris regilla) tadpoles. Archives of Environmental Contamination and Toxicology, 67: 444-452. doi: 10.1007/s00244-014-0062-2

Felsenberg, J., Gehring, K.B., Antemann, V. & Eisenhardt, D. (2011). Behavioural Pharmacology in Classical Conditioning of the Proboscis Extension Response in Honeybees (Apis mellifera). Journal of Visualized Experiments, e2282. doi: 10.3791/2282

Goñalons, C.M. & Farina, W.M. (2015). Effects of Sublethal Doses of Imidacloprid on Young Adult Honeybee Behaviour. PLoS One, 10: e0140814. doi: 10.1371/journal.pone.0140814

Goldberg, F., Grünewald, B., Rosenboom, H. & Menzel, R. (1999). Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera. The Journal of Physiology, 514: 759-768. doi: 10.1111/j.1469-7793.1999.759ad.x

Goulson, D., Nicholls, E., Botías, C. & Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347. doi: 10.1126/ science.1255957

Gregorc, A. & Ellis, J.D. (2011). Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pesticide Biochemistry and Physiology, 99: 200-207. doi: 10.1016/j.pestbp.2010.12.005

Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J.- F., Aupinel, P., Aptel, J., Tchamitchian, S. & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336: 348-350.doi: 10.1126/ science.1215039

Hepburn, H.R. & Radloff, S.E., 2011. Honeybees of Asia. Springer Science & Business Media, 239 p

Iqbal, J. & Mueller, U. (2007). Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society of London B: Biological Sciences, 274: 1517- 1521. doi: 10.1098/rspb.2007.0022

Iwasa, T., Motoyama, N., Ambrose, J.T. & Roe, R.M. (2004). Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection, 23: 371-378. doi:10.1016/j.cropro.2003.08.018

Jones, A.K., Raymond-Delpech, V., Thany, S.H., Gauthier, M. & Sattelle, D.B. (2006). The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Research, 16: 1422-1430. doi: 10.1101/gr.4549206

Levin, E.D., Swain, H.A., Donerly, S. & Linney, E. (2004). Developmental chlorpyrifos effects on hatchling zebrafish swimming behavior. Neurotoxicology and Teratology, 26: 719-723. doi: 10.1016/j.ntt.2004.06.013

Li, Z., Chen, Y., Zhang, S., Chen, S., Li, W., Yan, L., Shi, L., Wu, L., Sohr, A. & Su, S. (2013). Viral infection affects sucrose responsiveness and homing ability of forager honey bees, Apis mellifera L. PLoS One, 8: e77354. doi: 10.1371/ journal.pone.0077354

Li, Z., Liu, F., Li, W., Zhang, S., Niu, D., Xu, H., Hong, Q., Chen, S. & Su, S. (2012). Differential transcriptome profiles of heads from foragers: comparison between Apis mellifera ligustica and Apis cerana cerana. Apidologie, 43: 487-500. doi: 10.1007/s13592-012-0119-z

Müller, U. (2002). Learning in honeybees: from molecules to behaviour. Zoology, 105: 313-320. doi: 10.1078/0944-2006-00075

Menzel, R. & Muller, U. (1996). Learning and memory in honeybees: from behavior to neural substrates. Annual Review of Neuroscience, 19: 379-404. doi: 10.1146/annurev. ne.19.030196.002115

Mpumi, N., Mtei, K., Machunda, R. & Ndakidemi, P.A. (2016). The toxicity, persistence and mode of actions of selected botanical pesticides in Africa against insect pests in common beans, P. vulgaris: a review. American Journal of Plant Sciences, 07: 138-151. doi: 10.4236/ajps.2016.71015

Mullin, C.A., Frazier, M., Frazier, J.L., Ashcraft, S., Simonds, R. & Pettis, J.S. (2010). High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One, 5: e9754. doi: 10.1371/journal.pone.0009754

Neumann, P. & Carreck, N.L. (2010). Honey bee colony losses. Journal of Apicultural Research, 49: 1-6. doi: 10.3896/ IBRA.1.49.1.01

OECD (1998).Test no. 213: honeybees, acute oral toxicity test. OECD guidelines for the testing of chemicals, Section 2: 1-8.Retrived from: http:// www.oecd-ilibrary.org/environment/test-no-213-honeybees-acute-oral-toxicity-test_9789264070165-en

Palmer, M.J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G.A. & Connolly, C.N. (2013). Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nature Communications, 4: 1634. doi: 10.1038/ncomms2648

Park, D., Jung, J.W., Choi, B.-S., Jayakodi, M., Lee, J., Lim, J., Yu, Y., Choi, Y.-S., Lee, M.-L., Park, Y., Choi, I.Y., Yang, T.J., Edwards, O.R., Nah, G.J. & Kwon, H.W. (2015). Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing. BMC Genomics, 16: 1-16. doi: 10.1186/1471-2164-16-1

Peng, Y.-C. & Yang, E.-C. (2016). Sublethal Dosage of Imidacloprid Reduces the Microglomerular Density of Honey Bee Mushroom Bodies. Scientific Reports, 6: 19298. doi: 10.1038/srep19298

Pope, C.N. (1999). Organophosphorus pesticides: do they all have the same mechanism of toxicity? Journal of Toxicology and Environmental Health Part B: Critical Reviews, 2: 161- 181. doi: 10.1080/109374099281205

Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25: 345-353. doi: 10.1016/j.tree.2010.01.007

Qin, G., Liu, T., Guo, Y., Zhang, X., Ma, E. & Zhang, J. (2014). Effects of chlorpyrifos on glutathione S-transferase in migratory locust, Locusta migratoria. Pesticide Biochemistry and Physiology, 109: 1-5. doi: 10.1016/j.pestbp.2013.12.008

Reinhard, J., Srinivasan, M.V. & Zhang, S. (2004). Olfaction: scent-triggered navigation in honeybees. Nature, 427: 411- 411. doi: 10.1038/427411a

Suchail, S., Guez, D. & Belzunces, L.P. (2000). Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environmental Toxicology & Chemistry, 19:1901-1905. doi: 10.1002/etc.5620190726

Tan, K., Chen, W., Dong, S., Liu, X., Wang, Y. & Nieh, J.C. (2014). Imidacloprid Alters Foraging and Decreases Bee Avoidance of Predators. PLoS One, 9: e102725. doi: 10.1371/ journal.pone.0102725

Tan, K., Chen, W., Dong, S., Liu, X., Wang, Y. & Nieh, J.C. (2015). A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports, 5. doi: 10.1038/srep10989

Urlacher, E., Monchanin, C., Rivière, C., Richard, F.J., Lombardi, C., Michelsen-Heath, S., Hageman, K.J. & Mercer, A.R. (2016). Measurements of Chlorpyrifos Levels in Forager Bees and Comparison with Levels that Disrupt Honey Bee Odor-Mediated Learning Under Laboratory Conditions. Journal of Chemical Ecology, 42: 127-138. doi: 10.1007/s10886-016-0672-4

Vanengelsdorp, D. & Meixner, M. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103: S80. doi: 10.1016/j. jip.2009.06.011

Wang, Z. & Tan, K. (2014). Comparative analysis of olfactory learning of Apis cerana and Apis mellifera. Apidologie, 45: 45-52. doi: 10.1007/s13592-013-0228-3

Williamson, S.M., Moffat, C., Gomersall, M., Saranzewa, N., Connolly, C. & Wright, G.A. (2013). Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Frontiers in Physiology, 4: 13. doi: 10.3389/fphys.2013.00013

Wu, J.Y., Anelli, C.M. & Sheppard, W.S. (2011). Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS One, 6: e14720. doi: 10.1371/journal.pone.0014720

Yang, E.-C., Chang, H.-C., Wu, W.-Y. & Chen, Y.-W. (2012). Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS One, 7: e49472. doi: 10.1371/journal.pone.0049472

Yang, W., Kuang, H., Wang, S., Wang, J., Liu, W., Wu, Z., Tian, Y., Huang, Z.Y. & Miao, X. (2013). Comparative sucrose responsiveness in Apis mellifera and A. cerana foragers. PLoS One, 8: e79026. doi: 10.1371/journal.pone.0079026

Zhu, W., Schmehl, D.R., Mullin, C.A. & Frazier, J.L. (2014). Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS One, 9: e77547. doi: 10.1371/journal. pone.0077547181

Downloads

Published

2017-09-21

How to Cite

Li, Z., Li, M., Huang, J., Ma, C., Xiao, L., Huang, Q., Zhao, Y., Nie, H., & Su, S. (2017). Effects of Sublethal Concentrations of Chlorpyrifos on Olfactory Learning and Memory Performances in Two Bee Species, Apis mellifera and Apis cerana. Sociobiology, 64(2), 174–181. https://doi.org/10.13102/sociobiology.v64i2.1385

Issue

Section

Research Article - Bees

Most read articles by the same author(s)