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Volatile exposure within the honeybee hive and its effect on olfactory discrimination

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Abstract

Honeybees of different ages and reproductive castes cohabit in the hive where they are exposed to many odors that might affect associative learning. Our aim was to analyze the role of odors pre-exposed as volatiles on appetitive learning in honeybees of different ages and search for their long-term effect both under natural and laboratory conditions. By evaluating memory acquisition and retention through a differential proboscis extension response conditioning, we found that hive-exposed odors offered as a reinforced conditioned stimulus during training promoted a learning-reduced effect [latent inhibition (LI)]. On the other hand, no effect was found when the non-reinforced conditioned stimulus was pre-exposed. The LI effect varied with the odor identity. However, only slight differences were found with the age of the bees. Exposure-conditioning intervals longer than 24 h did not show an LI effect unless the odor concentration was increased or exposure was prolonged. Our results show that pre-exposed volatiles could either reduce learning performance, if this odor is later associated with food, or be irrelevant in the case that alternative scented resources circulate within the colony. The differential effects found according to the olfactory exposure characteristics could strongly influence the propagation of chemosensory information within the hive.

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Abbreviations

PER:

Proboscis extension response

US:

Unconditioned stimulus

CS:

Conditioned stimulus

LI:

Latent inhibition

References

  • Abramson CI, Bitterman ME (1986) Latent inhibition in honeybees. Anim Learn Behav 14:184–189

    Google Scholar 

  • Ackil JE, Mellgren RL (1968) Stimulus preexposure and instrumental learning. Psychon Sci 11:339

    Google Scholar 

  • Ackil JE, Mellgren RL, Halgren C, Frommer GP (1969) Effects of CS preexposure on avoidance learning in rats with hippocampal lesions. J Comp Physiol Psychol 69:739–747

    Article  PubMed  CAS  Google Scholar 

  • Arenas A, Farina WM (2008) Age and rearing environment interact in the retention of early olfactory memories in honeybees. J Comp Physiol A 194:629–640

    Article  Google Scholar 

  • Arenas A, Fernandez VM, Farina WM (2008) Floral scents experienced within the colony affect long-term foraging preferences in honeybees. Apidologie 39:714–722

    Article  Google Scholar 

  • Bitterman ME, Menzel R, Fietz A, Schaefer S (1983) Classical conditioning of proboscis extension in honeybees. J Comp Physiol A 97:107–119

    CAS  Google Scholar 

  • Blodgett HC (1929) The effect of the introduction of reward upon the maze performance of rats. Univ Calif Publ Psychol 4:113–134

    Google Scholar 

  • Bouton ME, Moody EW (2004) Memory processes in classical conditioning. (Special issue: neurobiology of cognition in laboratory animals: challenges and opportunities). Neurosci Biobehav Rev 28:663–674

    Article  PubMed  Google Scholar 

  • Breed MD, Perry S, Bjostad LB (2004) Testing the blank slate hypothesis: why honeybee colonies accept young bees. Insectes Soc 51:1216

    Article  Google Scholar 

  • Carlton PL, Vogel JR (1967) Habituation and conditioning. J Comp Physiol Psychol 63:348–351

    Article  PubMed  CAS  Google Scholar 

  • Chandra SBC, Hosler JS, Smith BH (2000) Heritable variation for latent inhibition and its correlation to reversal learning in the honeybee, Apis mellifera. J Comp Psychol 114:86–97

    Article  PubMed  CAS  Google Scholar 

  • Daly KC, Durtschi ML, Smith BH (2001) Olfactory-based discrimination in the moth, Manduca sexta. J Insect Physiol 47:375–384

    Article  PubMed  CAS  Google Scholar 

  • Farina WM, Grüter C, Díaz PC (2005) Social learning of floral odours inside the honeybee hive. Proc R Soc Lond B Biol Sci 272:1923–1928

    Article  Google Scholar 

  • Farina WM, Grüter C, Acosta LE, McCabe S (2007) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94:55–60

    Article  PubMed  CAS  Google Scholar 

  • Ferguson HJ, Cobey S, Smith BH (2001) Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera. Anim Behav 61:527–534

    Article  Google Scholar 

  • Franks NR, Hooper JW, Dornhaus A, Aukett PJ, Hayward AL, Berghoff S (2007) Reconnaissance and latent learning in ants. Proc R Soc B 274:1505–1509

    Article  PubMed  Google Scholar 

  • Gerber B, Geberzahn N, Hellstern F, Klein J, Kowalksy O, Wüstenberg D, Menzel R (1996) Honeybees transfer olfactory memories established during flower visits to a proboscis extension paradigm in the laboratory. Anim Behav 52:1079–1085

    Article  Google Scholar 

  • Getz WM, Smith KB (1991) Olfactory perception in honeybees: concatenated and mixed odorant stimuli, concentration, and exposure effects. J Comp Physiol A 169:215–230

    Article  Google Scholar 

  • Goyret J, Farina WM (2005) Non-random nectar unloading interactions between foragers and their receivers in the honeybee hive. Naturwissenschaften 92:440–443

    Article  PubMed  CAS  Google Scholar 

  • Grüter C, Farina WM (in press) Social experiences affect interaction patterns amongst foragers and hive mates in honeybees. Ethology

  • James JP (1971) Latent inhibition and the preconditioning interval. Psychon Sci 24:97–98

    Google Scholar 

  • Knudsen JT, Tollsten L, Bergstrom LG (1993) Floral scents—a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33:253–280

    Article  CAS  Google Scholar 

  • Konorski J, Szwejkowska G (1952) Chronic extinction and restoration of conditioned reflexes. IV. The dependence of the course of extinction and restoration of conditioned reflexes on the history of the conditioned stimulus (the principle of primacy of first training). Acta Biol Exp 16:95–113

    Google Scholar 

  • Laloi D, Pham-Delègue MH (2004) Bumble bees show asymmetrical discrimination between two odors in a classical conditioning procedure. J Insect Behav 17(3):385–396

    Article  Google Scholar 

  • Lubow RE (1965) Latent inhibition: effects of frequency of non-reinforced preexposure to the CS. J Comp Physiol Psychol 60:454–455

    Article  PubMed  CAS  Google Scholar 

  • Lubow RE (1973) Latent inhibition. Psychol Bull 79(6):398–407

    Article  PubMed  CAS  Google Scholar 

  • Lubow KE, Moore AU (1959) Latent inhibition: the effect of nonreinforced pre-exposure to the conditional stimulus. J Comp Physiol Psychol 52:416–419

    Article  Google Scholar 

  • Lubow RE, Siebert L (1969) Latent inhibition within the CER paradigm. J Comp Physiol Psychol 68:136–138

    Article  PubMed  CAS  Google Scholar 

  • Lubow RE, Markhan RE, Allen J (1968) Latent inhibition and classical conditioning of the rabbit pinna response. J Comp Physiol Psychol 60:454–455

    Article  Google Scholar 

  • Lunney GH (1970) Using analysis of variance with a dichotomous dependent variable: an empirical study. J Educ Meas 7:263–269

    Article  Google Scholar 

  • Mackintosh NJ (1975) A theory of attention: variations in the associability of stimuli with reinforcement. Psychol Rev 82:276–298

    Article  Google Scholar 

  • Michener CD (1974) The social behavior of bees: a comparative study. Harvard University Press, Cambridge

    Google Scholar 

  • Reiss S, Wagner AR (1972) CS habituation produces a “latent inhibition effect” but no active “conditioned inhibition”. Learn Motiv 3:237–245

    Article  Google Scholar 

  • Sandoz JC, Laloi D, Odoux JF, Pham-Delègue MH (2000) Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure. Anim Behav 59:1025–1034

    Article  PubMed  Google Scholar 

  • Seeley TD (1995) The wisdom of the hive: the social physiology of honeybee colonies. Harvard University Press, Cambridge

    Google Scholar 

  • Siegel S (1970) Retention of latent inhibition. Psychon Sci 20:161–162

    Google Scholar 

  • Sokal RR, Rohlf FJ (2000) Biometry: the principles and practice of statistics in biological research. State University of New York, New York

    Google Scholar 

  • Suboski MD, Di Lollo V, Gormezano I (1964) Effects of unpaired preacquisition exposure of CS and UCS on classical conditioning of the nictitating membrane response of the albino rabbit. Psychol Rep 15:571–576

    Google Scholar 

  • Takeda K (1961) Classical conditioned response in the honeybee. J Insect Physiol 6:168–179

    Article  CAS  Google Scholar 

  • Tolman EC, Honzik CH (1930) Introduction and removal of reward, and maze performance in rats. U Cal Pub Psych 4:257–275

    Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

We thank the two anonymous referees for their valuable comments and suggestions that improved the final version of this manuscript. This study was supported by grants from ANPCYT (01-1155), University of Buenos Aires (X 077) and CONICET to WMF. We declare that our experiments comply with the current laws of the country in which they were performed.

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Authors and Affiliations

  1. Grupo de Estudio de Insectos Sociales, IFIBYNE-CONICET, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria, C1428EHA, Buenos Aires, Argentina

    Vanesa M. Fernández, Andrés Arenas & Walter M. Farina

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  1. Vanesa M. Fernández
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  2. Andrés Arenas
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  3. Walter M. Farina
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Correspondence to Walter M. Farina.

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Fernández, V.M., Arenas, A. & Farina, W.M. Volatile exposure within the honeybee hive and its effect on olfactory discrimination. J Comp Physiol A 195, 759–768 (2009). https://doi.org/10.1007/s00359-009-0453-4

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