Learning and Discrimination of Individual Cuticular Hydrocarbons by Honeybees (Apis mellifera)

Châline, Nicolas; Sandoz, Jean‐Christophe; Martin, Stephen J.; Ratnieks, Francis L. W.; Jones, Graeme R.

doi:10.1093/chemse/bji027

Cited by 109 publications

(93 citation statements)

References 33 publications

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“…Olfactory PER conditioning has become a versatile tool for the study of questions, not only in the field of comparative experimental psychology (e.g., Chandra and Smith 1998;Hellstern et al 1998;Deisig et al 2001Deisig et al , 2002Deisig et al , 2003, as originally planned by Takeda, but also in diversified fields such as olfactory perception (e.g., Vareschi 1971;Guerrieri et al 2005b;Reinhard et al 2010), neurobiology of olfaction and olfactory learning (e.g., Hammer 1993;Stopfer et al 1997;Faber et al 1999;Sandoz et al 2003;Rath et al 2011), molecular bases of memory (for review, see Menzel 1999;Schwärzel and Müller 2006), social bases of behavior in bees (e.g., Chaline et al 2005;Arenas and Farina 2008), and floral ecology (Wright et al 2002(Wright et al , 2005, to cite only a few examples. The basic premises of olfactory PER conditioning have also been adapted in other species, such as bumblebees (Laloi et al 1999;Riveros and Gronenberg 2009), stingless bees (McCabe et al 2007;Farina 2009, 2010), moths (Fan et al 1997;Fan and Hansson 2001;Daly et al 2004), and even ants, which do not have a proboscis but whose mouthpart movements can also be conditioned (Guerrieri and d'Ettorre 2010;Guerrieri et al 2011).…”

Section: Resultsmentioning

confidence: 99%

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Giurfa

Sandoz²

2012

Learn. Mem.

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352

334

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The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.Classical conditioning (Pavlov 1927) is a form of conditioning in which a subject learns to associate a neutral stimulus (the "conditioned stimulus," or CS), which does not originally elicit a behavioral response, with a stimulus of biological significance (the "unconditioned stimulus," or US), which elicits an innate, often reflexive, response. Through this association, the originally neutral stimulus acquires the capacity to elicit a conditioned response.Decades of research on animal learning and memory have established some invertebrates (e.g., the sea hare, Aplysia californica, the fruit fly, Drosophila melanogaster, the honeybee, Apis mellifera) as standard models for the study of classical conditioning (Giurfa 2007b;Menzel et al. 2007). This success can be attributed to the fact that these animals can learn nonassociative as well as Pavlovian and operant associations and possess relatively simple nervous systems that allow retracing of these phenomena to the cellular and molecular levels in different kinds of laboratory preparations. Among these invertebrates, the honeybee, Apis mellifera, has emerged as a robust and influential model for the study of

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Section: Resultsmentioning

confidence: 99%

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Giurfa

Sandoz²

2012

Learn. Mem.

Self Cite

352

334

View full text Add to dashboard Cite

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“…Analyses show that their composition varies less within a colony than between different colonies Singer, 1998). Of the different categories of hydrocarbons, alkenes might be of more biological relevance than alkanes (Dani, 2005), and workers have been shown to be able to discriminate alkenes better than alkanes (Chaline et al, 2005). Of interest to us, however, would be compounds that differ between the cuticles of honey bee and the common wasp workers (Butts et al, 1991;Steinmetz et al, 2003, Dani et al, 2004Dani, 2005).…”

Section: Discussionmentioning

confidence: 99%

Recognition errors by honey bee (Apis mellifera) guards demonstrate overlapping cues in conspecific recognition

Couvillon¹,

Roy²,

Ratnieks³

2009

J. of Api. Res

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SummaryHoney bee (Apis mellifera) entrance guards discriminate nestmates from intruders. We tested the hypothesis that the recognition cues between nestmate bees and intruder bees overlap by comparing their acceptances with that of worker common wasps, Vespula vulgaris, by entrance guards. If recognition cues of nestmate and non-nestmate bees overlap, we would expect recognition errors. Conversely, we hypothesised that guards would not make errors in recognizing wasps because wasps and bees should have distinct, non-overlapping cues. We found both to be true. There was a negative correlation between errors in recognizing nestmates (error: reject nestmate) and nonnestmates (error: accept non-nestmate) bees such that when guards were likely to reject nestmates, they were less likely to accept a nonnestmate; conversely, when guards were likely to accept a non-nestmate, they were less likely to reject a nestmate. There was, however, no correlation between errors in the recognition of nestmate bees (error: reject nestmate) and wasps (error: accept wasp), demonstrating that guards were able to reject wasps categorically. Our results strongly support that overlapping cue distributions occur, resulting in errors and leading to adaptive shifts in guard acceptance thresholds

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“…Furthermore, the stinger discharges alarm pheromones (primarily isoamyl acetate) after it has been embedded in the opponent. The worker bee is characterized by a stagespecific profile of C21-C33 cuticular hydrocarbons and pheromones, including eicosenol, ethyl oleate, and 10-hydroxy-decenoic acid that changes as a function of the social role of the animal (Chaline et al, 2005;Dor et al, 2005;Leoncini et al, 2004a,b).…”

Section: A Anatomy Of Individualsmentioning

confidence: 99%

Order, Disorder, Death: Lessons from a Superorganism

Amdam¹,

Seehuus²

2006

Advances in Cancer Research

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Animal models contribute to the understanding of molecular mechanism of cancer, revealing complex roles of altered cellular-signaling networks and deficient surveillance systems. Analogous pathologies are documented in an unconventional model organism that receives attention in research on systems theory, evolution, and aging. The honeybee (Apis mellifera) colony is an advanced integrative unit, a "superorganism" in which order is controlled via complex signaling cascades and surveillance schemes. A facultatively sterile caste, the workers, regulates patterns of growth, differentiation, homeostasis, and death. Workers differentiate into temporal phenotypes in response to dynamic social cues; chemosensory signals that can translate into dramatic physiological responses, including programmed cell death. Temporal worker forms function together, and effectively identify and terminate abnormal colony members ranging from embryos to adults. As long as this regulatory system is operational at a colony level, the unit survives and propagates. However, if the worker phenotypes that collectively govern order become too few or change into malignant forms that bypass control mechanisms to replicate aberrantly; order is replaced by disorder that ultimately leads to the destruction of the society. In this chapter we describe fundamental properties of honeybee social organization, and explore conditions that lead to states of disorder. Our hope is that this chapter will be an inspirational source for ongoing and future work in the field of cancer research.

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Learning and Discrimination of Individual Cuticular Hydrocarbons by Honeybees (Apis mellifera)

Cited by 109 publications

References 33 publications

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees

Recognition errors by honey bee (Apis mellifera) guards demonstrate overlapping cues in conspecific recognition

Order, Disorder, Death: Lessons from a Superorganism

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