Effect of Flumethrin on Survival and Olfactory Learning in Honeybees

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Abstract

Flumethrin has been widely used as an acaricide for the control of Varroa mites in commercial honeybee keeping throughout the world for many years. Here we test the mortality of the Asian honeybee Apis cerana cerana after treatment with flumethrin. We also ask (1) how bees react to the odor of flumethrin, (2) whether its odor induces an innate avoidance response, (3) whether its taste transmits an aversive reinforcing component in olfactory learning, and (4) whether its odor or taste can be associated with reward in classical conditioning. Our results show that flumethrin has a negative effect on Apis ceranàs lifespan, induces an innate avoidance response, acts as a punishing reinforcer in olfactory learning, and interferes with the association of an appetitive conditioned stimulus. Furthermore flumethrin uptake within the colony reduces olfactory learning over an extended period of time.

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Most cited references 19

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Classical conditioning of proboscis extension in honeybees (Apis mellifera).

M E Bitterman, R. Menzel, A Fietz … (1983)

Extension of the proboscis was conditioned in restrained honeybees with odor as the conditioned stimulus (CS) and sucrose solution--delivered to the antenna (to elicit extension of the proboscis) and then to the proboscis itself--as the unconditioned stimulus (US). In a first series of experiments, acquisition was found to be very rapid, both in massed and in spaced trials; its associative basis was established by differential conditioning and by an explicitly unpaired control procedure (which produced marked resistance to acquisition in subsequent paired training); and both extinction and spontaneous recovery in massed trials were demonstrated. In a series of experiments on the nature of the US, eliminating the proboscis component was found to lower the asymptotic level of performance, whereas eliminating the antennal component was without effect; reducing the concentration of sucrose from 20% to 7% slowed acquisition but did not lower the asymptotic level of performance; and second-order conditioning was demonstrated. In a series of experiments on the role of the US, an omission contingency designed to eliminate adventitious response-reinforcer contiguity was found to have no adverse effect on acquisition. In a series of experiments designed to analyze the resistance to acquisition found after explicitly unpaired training in the first experiments, no significant effect was found of prior exposure either to the CS alone or to the US alone, although the unpaired procedure again produced substantial resistance that was shown to be due to inhibition rather than to inattention; extinction after paired training was found to be facilitated by unpaired presentations of the US. The relation between these results for honeybees and those of analogous experiments with vertebrates is considered.

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DDT, pyrethrins, pyrethroids and insect sodium channels.

Peter N R Usherwood, Suzanne Field, Susan E. Davies … (2007)

The long term use of many insecticides is continually threatened by the ability of insects to evolve resistance mechanisms that render the chemicals ineffective. Such resistance poses a serious threat to insect pest control both in the UK and worldwide. Resistance may result from either an increase in the ability of the insect to detoxify the insecticide or by changes in the target protein with which the insecticide interacts. DDT, the pyrethrins and the synthetic pyrethroids (the latter currently accounting for around 17% of the world insecticide market), act on the voltage-gated sodium channel proteins found in insect nerve cell membranes. The correct functioning of these channels is essential for normal transmission of nerve impulses and this process is disrupted by binding of the insecticides, leading to paralysis and eventual death. Some insect pest populations have evolved modifications of the sodium channel protein which prevent the binding of the insecticide and result in the insect developing resistance. Here we review some of the work (done at Rothamsted Research and elsewhere) that has led to the identification of specific residues on the sodium channel that may constitute the DDT and pyrethroid binding sites.

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Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior.

Yassine Aliouane, Sayed Hassani, Vincent Gary … (2008)

Laboratory bioassays were conducted to evaluate the effects on honeybee behavior of sublethal doses of insecticides chronically administered orally or by contact. Emergent honeybees received a daily dose of insecticide ranging from one-fifth to one-five-hundredth of the median lethal dose (LD50) during 11 d. After exposure to fipronil (0.1 and 0.01 ng/bee), acetamiprid (1 and 0.1 microg/bee), or thiamethoxam (1 and 0.1 ng/bee), behavioral functions of honeybees were tested on day 12. Fipronil, used at the dose of 0.1 ng/bee, induced mortality of all honeybees after one week of treatment. As a result of contact treatment at 0.01 ng/bee, honeybees spent significantly more time immobile in an open-field apparatus and ingested significantly more water. In the olfactory conditioning paradigm, fipronil-treated honeybees failed to discriminate between a known and an unknown odorant. Thiamethoxam by contact induced either a significant decrease of olfactory memory 24 h after learning at 0.1 ng/bee or a significant impairment of learning performance with no effect on memory at 1 ng/bee. Responsiveness to antennal sucrose stimulation was significantly decreased for high sucrose concentrations in honeybees treated orally with thiamethoxam (1 ng/bee). The only significant effect of acetamiprid (administered orally, 0.1 microg/bee) was an increase in responsiveness to water. The neonicotinoids acetamiprid and thiamethoxam tested at the highest dose (one-tenth and one-fifth of their oral LD50, respectively) and fipronil at one-five-hundredth of LD50 have limited effects on the motor, sensory, and cognitive functions of the honeybee. Our data on the intrinsic toxicity of the compounds after chronic exposure have to be taken into account for evaluation of risk to honeybees in field conditions.

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Author and article information

Contributors

Frederic Marion-Poll: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 13 June 2013

Volume: 8

Issue: 6

Electronic Location Identifier: e66295

Affiliations

[1 ]Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, Kunming, China

[2 ]Eastern Bee Research Institute, Yunnan Agricultural University, Kunming, China

[3 ]Institut of Biologie and Neurobiology, Freie Universität Berlin, Berlin, Germany

AgroParisTech, France

Author notes

* E-mail: kentan@ 123456xtbg.ac.cn

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: KT SY ZWW RM. Performed the experiments: KT SY ZWW. Analyzed the data: KT ZWW RM. Contributed reagents/materials/analysis tools: KT ZWW. Wrote the paper: KT ZWW RM.

Article

Publisher ID: PONE-D-12-35945

DOI: 10.1371/journal.pone.0066295

PMC ID: 3681914

PubMed ID: 23785490

SO-VID: aa2de6ee-8a06-4baa-babb-45d5c65299ad

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This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 16 November 2012

Date accepted : 6 May 2013

Page count

Pages: 7

Funding

This work was supported by the Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, China National Research Fund (31260585) and China National Agricultural Production Systematic Fund (CARS-45-kxj14). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Effect of Flumethrin on Survival and Olfactory Learning in Honeybees

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Abstract

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Teaching and learning evolution

Most cited references 19

Classical conditioning of proboscis extension in honeybees (Apis mellifera).

DDT, pyrethrins, pyrethroids and insect sodium channels.

Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior.

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