全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Imidacloprid Alters Foraging and Decreases Bee Avoidance of Predators

DOI: 10.1371/journal.pone.0102725

Full-Text   Cite this paper   Add to My Lib

Abstract:

Concern is growing over the effects of neonicotinoid pesticides, which can impair honey bee cognition. We provide the first demonstration that sublethal concentrations of imidacloprid can harm honey bee decision-making about danger by significantly increasing the probability of a bee visiting a dangerous food source. Apis cerana is a native bee that is an important pollinator of agricultural crops and native plants in Asia. When foraging on nectar containing 40 μg/L (34 ppb) imidacloprid, honey bees (Apis cerana) showed no aversion to a feeder with a hornet predator, and 1.8 fold more bees chose the dangerous feeder as compared to control bees. Control bees exhibited significant predator avoidance. We also give the first evidence that foraging by A. cerana workers can be inhibited by sublethal concentrations of the pesticide, imidacloprid, which is widely used in Asia. Compared to bees collecting uncontaminated nectar, 23% fewer foragers returned to collect the nectar with 40 μg/L imidacloprid. Bees that did return respectively collected 46% and 63% less nectar containing 20 μg/L and 40 μg/L imidacloprid. These results suggest that the effects of neonicotinoids on honey bee decision-making and other advanced cognitive functions should be explored. Moreover, research should extend beyond the classic model, the European honey bee (A. mellifera), to other important bee species.

References

[1]  Lonsdorf E, Ricketts T, Kremen C, Winfree R, Greenleaf S, et al. (2011) Crop pollination services. In: Karieva P, Tallis H, Ricketts T, Daily GC, Polasky S, editors. Natural capital: theory and practice of mapping ecosystem services. Oxford: Oxford University Press. 168–187.
[2]  Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, et al. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol (Amst) 25: 345–353 doi:10.1016/j.tree.2010.01.007.
[3]  Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52: 81–106 doi:10.1146/annurev.ento.52.110405.091440.
[4]  Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336: 351–352 doi:10.1126/science.1215025.
[5]  Cresswell JE, Desneux N, vanEngelsdorp D (2012) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Manag Sci 68: 819–827 doi:10.1002/ps.3290.
[6]  Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50: 977–987 doi:10.1111/1365-2664.12111.
[7]  Jeschke P, Nauen R (2008) Neonicotinoids–from zero to hero in insecticide chemistry. Pest Manag Sci 64: 1084–1098. doi: 10.1002/ps.1631
[8]  Gross M (2013) EU ban puts spotlight on complex effects of neonicotinoids. Curr Biol.
[9]  Abrol DP (2013) Safety of bees in relation to pest management. Asiatic Honeybee Apis cerana. Dordrecht: Springer Netherlands. 575–640. doi:10.1007/978-94-007-6928-1_14.
[10]  Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity–USA. Apidologie 41: 312–331 doi:10.1051/apido/2010018.
[11]  Decourtye A, Henry M, Desneux N (2013) Environment: overhaul pesticide testing on bees. Nature 497: 188 doi:10.1038/497188a.
[12]  Schmuck R, Nauen R, Ebbinghaus-Kintscher U (2003) Effects of imidacloprid and common plant metabolites of imidacloprid in the honeybee: toxicological and biochemical considerations. Bull Insectol 56: 27–34.
[13]  Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotox Environ Safe 57: 410–419 Available: http://www.sciencedirect.com/science/art?icle/pii/S0147651303001477.
[14]  Decourtye A, Lacassie E, Pham-Delègue MH (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59: 269–278 doi:10.1002/ps.631.
[15]  Ramirez-Romero R, Chaufaux J, Pham-Delègue MH (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36: 601–611 doi:10.1051/apido:2005039.
[16]  Lambin M, Armengaud C, Raymond S, Gauthier M (2001) Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch Insect Biochem Physiol 48: 129–134 doi:10.1002/arch.1065.
[17]  Schneider CW, Tautz JR, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLOS ONE 7: e30023 doi:10.1371/journal.pone.0030023.g005.
[18]  Henry M, Beguin M, Requier F, Rollin O, Odoux JF, et al. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336: 348–350 doi:10.1126/science.1215039.
[19]  Pahl M, Tautz JR, Zhang SW (2010) Honeybee cognition. Animal Behaviour: Evolution and Mechanisms. Berlin: Springer. 87–120. doi:10.1007/978-3-642-02624-9_4.
[20]  Williamson SM, Baker DD, Wright GA (2012) Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera. Invert Neurosci 13: 63–70 doi:10.1007/s10158-012-0144-7.
[21]  Yang EC, Chang HC, Wu WY, Chen YW (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
[22]  Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010) Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotox. 19: 1612–1619 doi:10.1007/s10646-010-0546-4.
[23]  Eiri DM, Nieh JC (2012) A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. J Exp Biol 215: 2022–2029 doi:10.1242/jeb.068718.
[24]  Gon?alves-Souza T, Omena PM, Souza JC, Romero GQ (2008) Trait-mediated effects on flowers: artificial spiders deceive pollinators and decrease plant fitness. Ecology 89: 2407–2413. doi: 10.1890/07-1881.1
[25]  Dukas R, Morse DH (2005) Crab spiders show mixed effects on flower-visiting bees and no effect on plant fitness components. Ecoscience 12: 244–247. doi: 10.2980/i1195-6860-12-2-244.1
[26]  Bray A, Nieh JC (2014) Non-consumptive predator effects shape honey bee foraging and recruitment dancing. PLOS ONE 9: e87459 doi:10.1371/journal.pone.0087459.
[27]  Abrol DP (2006) Defensive behaviour of Apis cerana F. against predatory wasps. J Apic Sci 20: 39–46.
[28]  Burgett M, Akratanakul P (1982) Predation on the western honey bee, Apis mellifera L., by the hornet, Vespa tropica (L.). Psyche 89: 347–350 doi:10.1155/1982/37970.
[29]  Matsuura M, Yamane S (1990) Biology of the vespine wasps. Berlin, Germany: Springer Verlag. 1 p.
[30]  Tan K, Li H, Yang MX, Hepburn HR, Radloff SE (2010) Wasp hawking induces endothermic heat production in guard bees. J Insect Sci 10: 1–6 doi:10.1673/031.010.14102.
[31]  Tan K, Radloff SE, Li JJ, Hepburn HR, Yang MX, et al. (2007) Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 94: 469–472 Available: http://www.springerlink.com/index/10.100?7/s00114-006-0210-2.
[32]  Tan K, Hu Z, Chen W, Wang Y, Wang Z, et al. (2013) Fearful foragers: honey bees tune colony and individual foraging to multi-predator presence and food quality. PLOS ONE 8: e75841. doi: 10.1371/journal.pone.0075841
[33]  Tomé HVV, Martins GF, Lima MAP, Campos LAO, Guedes RNC (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLOS ONE 7: e38406 doi:10.1371/journal.pone.0038406.
[34]  Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature: 1–5. doi:10.1038/nature11585.
[35]  Arena M, Sgolastra F (2014) A meta-analysis comparing the sensitivity of bees to pesticides. Ecotox 23: 324–334. doi: 10.1007/s10646-014-1190-1
[36]  Verma LR, Partap U (1993) The Asian hive bee, Apis cerana, as a pollinator in vegetable seed production. International Centre for Integrated Mountain Development (ICIMOD).
[37]  Yang GH (2005) Harm of introducing the western honey bee, Apis mellifera L., to the Chinese honey bee Apis cerana F. and its ecological impact. Acta Entomol Sinica (Chinese language journal) 48: 401–406.
[38]  Corlett RT (2001) Pollination in a degraded tropical landscape: a Hong Kong case study. J Trop Ecol 17: 155–161 doi:10.1017/S0266467401001109.
[39]  Peng YS, Nasr ME, Locke SJ (1989) Geographical races of Apis cerana Fabricius in China and their distribution. Review of recent Chinese publications and a preliminary statistical analysis. Apidologie 20: 9–20. doi: 10.1051/apido:19890102
[40]  Higo M (1980) Sensitivity of honeybees to some pesticides with special reference to the effects of age and season. Honeybee Sci 1: 177–180.
[41]  Suh YT, Shim JH (1988) A study on the enzyme activities of a honeybee (Apis cerana F.) associated with the degradation of some insecticides. Korean J Environ Agric 8: 47–54.
[42]  Mishra RC, Verma AK (1982) Relative toxicity of some insecticides to Apis cerana indica F. workers. Indian Bee J 44: 475–476.
[43]  Khan RB, Dethe MD (2005) Toxicity of new pesticides to honey bees. In: Kumar A, editor. Environment and Toxicology. New Delhi: APH Publishing Corporation. 59–62.
[44]  Yuchong W, Weiwen C, Shihao D, Xiwen L, Ken T (2014) Toxicity of imidacloprid to honeybee (Apis cerana). J Yunnan Agricul Univ: inpress.
[45]  Yu X, Wang M, Kang M, Liu L, Guo X, et al. (2011) Molecular cloning and characterization of two nicotinic acetylcholine receptor β subunit genes from Apis cerana cerana. Arch Insect Biochem Physiol 77: 163–178. doi: 10.1002/arch.20432
[46]  Sun ZJ, Fang XC, Du WZ (1995) Imidacloprid as a highly efficient pesticide. J Plant Protect 2: 44–45.
[47]  Monceau K, Bonnard O, Thiéry D (2014) Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci 87: 1–16 doi:10.1007/s10340-013-0537-3.
[48]  Bubník Z, Kadlec P, Urban D, Bruhns M (1995) Sugar technologists manual: Chemical and physical data for sugar manufacturers and users. Verlag Dr Albert Bartens 120: 574–575.
[49]  Byrne FJ, Visscher PK, Leimkuehler B, Fischer D, Grafton-Cardwell EE, et al. (2013) Determination of exposure levels of honey bees foraging on flowers of mature citrus trees previously treated with imidacloprid. Pest Manag Sci. doi:10.1002/ps.3596.
[50]  Cresswell JE (2010) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotox 20: 149–157 doi:10.1007/s10646-010-0566-0.
[51]  Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216: 1799–1807 doi:10.1242/jeb.083931.
[52]  Belzunces LP, Tchamitchian S, Brunet JL (2012) Neural effects of insecticides in the honey bee. Apidologie 43: 348–370 doi:10.1007/s13592-012-0134-0.
[53]  Schmuck R, Sch?ning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57: 225–238 doi:10.1002/ps.270.
[54]  Nauen R, Ebbinghaus-Kintscher U, Schmuck R (2001) Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag Sci 57: 577–586 doi:10.1002/ps.331.
[55]  Zar JH (1984) Biostatistical analysis. Englewood Cliffs, New Jersey: Prentice-Hall.
[56]  Colin ME, Bonmatin JM, Moineau I, Gaimon C, Brun S, et al. (2004) A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch Environ Contam Toxicol 47. doi:10.1007/s00244-004-3052-y.
[57]  Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101: 1743–1748. doi: 10.1603/0022-0493-101.6.1743
[58]  Suchail S, Debrauwer L, Belzunces LP (2004) Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 60: 291–296. doi: 10.1002/ps.772
[59]  Schricker B, Stephen WP (1970) The effect of sublethal doses of parathion on honeybee behaviour. I. Oral administration and the communication dance. Journal of Apicultural Research 9: 141–153.
[60]  Barron AB, Maleszka R, Vander Meer RK, Robinson GE (2007) Octopamine modulates honey bee dance behavior. Proc Natl Acad Sci USA 104: 1703–1707 doi:10.1073/pnas.0610506104.
[61]  Landgraf T, Rojas R, Nguyen H, Kriegel F, Stettin K (2011) Analysis of the waggle dance motion of honeybees for the design of a biomimetic honeybee robot. PLOS ONE 6: e21354 doi:10.1371/journal.pone.0021354.t001.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133