Skip to main content

Comparison of learning and memory of Apis cerana and Apis mellifera

Journal of Comparative Physiology A volume 198, pages 777–786 (2012)Cite this article

Abstract

The honeybee is an excellent model organism for research on learning and memory among invertebrates. Learning and memory in honeybees has intrigued neuroscientists and entomologists in the last few decades, but attention has focused almost solely on the Western honeybee, Apis mellifera. In contrast, there have been few studies on learning and memory in the Eastern honeybee, Apis cerana. Here we report comparative behavioral data of color and grating learning and memory for A. cerana and A. mellifera in China, gathered using a Y-maze apparatus. We show for the first time that the learning and memory performance of A. cerana is significantly better on both color and grating patterns than that of A. mellifera. This study provides the first evidence of a learning and memory difference between A. cerana and A. mellifera under controlled conditions, and it is an important basis for the further study of the mechanism of learning and memory in honeybees.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

A. mellifera :

Apis mellifera

A. cerana :

Apis cerana

CCD:

Colony collapse disorder

References

  • Avargues-Weber A, Dyer AG, Giurfa M (2011) Conceptualization of above and below relationships by an insect. Proc R Soc Lond Ser B 278:898–905

    Article  Google Scholar 

  • Avargues-Weber A, Dyer AG, Combe M, Giurfa M (2012) Simultaneous mastering of two abstract concepts by the miniature brain of bees. Proc Natl Acad Sci 109:7481–7486

    PubMed  Article  CAS  Google Scholar 

  • Baird E, Srinivasan M, Zhang S, Cowling A (2005) Visual control of flight speed in honeybees. J Exp Biol 208:3895

    PubMed  Article  Google Scholar 

  • Butler CG (1975) The honey bee colony-life history. In: The Hive and the Honey Bee. Dadant and Sons, Hamilton, pp 39–74

  • Chandra BCS, Geetha L, Abraham VA, Karanth P, Thomas K, Srinivasan MV, Gadagkar R (1998) Uniform discrimination of pattern orientation by honeybees. Anim Behav 56:1391–1398

    Article  Google Scholar 

  • Chen S (2001) The apicultural science in China. China Agriculture Press, Beijing

    Google Scholar 

  • Chen L, Zhang S, Srinivasan M (2003) Global perception in small brains: topological pattern recognition in honey bees. Proc Natl Acad Sci 100:6884

    PubMed  Article  CAS  Google Scholar 

  • Cheng W, Zhou C, Chai H, Zhao S, Li B (2009) Quantitative extraction and analysis of basic morphological types of land geomorphology in China. J Geo-Inf Sci 6:725–736

    Google Scholar 

  • Chittka L, Vorobyev M, Shmida A, Menzel R (1993) Bee color vision—the optimal system for the discrimination of flower colours with three spectral photoreceptor types? In: Wiese K (ed) Sensory systems of Arthropods. Springer-Verlag, New York, pp 211–218

    Google Scholar 

  • Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics: bees trade off foraging speed for accuracy. Nature 424:388

    PubMed  Article  CAS  Google Scholar 

  • Collett TS, Graham P, Durier V (2003) Route learning by insects. Curr Opin Neurobiol 13:718–725

    PubMed  Article  CAS  Google Scholar 

  • De Ibarra NH, Vorobyev M, Brandt R, Giurfa M (2000) Detection of bright and dim colours by honeybees. J Exp Biol 203:3289–3298

    Google Scholar 

  • Dietz A, Krell R, Pettis J (1986) The potential limit of survival for Africanized bees in the United States. In: Proceeding of the Africanized Honey Bee Symposium, American Farm Bureau Research Foundation, Atlanta, GA, Feb 11–12, pp 87–100

  • Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y, Underwood R (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4:e6481

    PubMed  Article  Google Scholar 

  • Fan Y, Zhou M (2005) World Atlas. China Map Press, Beijing

    Google Scholar 

  • Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 91:228–231

    PubMed  Article  CAS  Google Scholar 

  • Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801–824

    Article  Google Scholar 

  • Giurfa M, Eichmann B, Menzel R (1996) Symmetry perception in an insect. Nature 382:458–461

    PubMed  Article  CAS  Google Scholar 

  • Giurfa M, Vorobyev M, Brandt R, Posner B, Menzel R (1997) Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. J Comp Physiol A 180:235–243

    Article  Google Scholar 

  • Giurfa M, Zhang S, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410:930–932

    PubMed  Article  CAS  Google Scholar 

  • Gong Y, Zhang Q (2000) Classification and evolution of honeybee. Fujian science and technology press, Fuzhou

    Google Scholar 

  • Gross HJ, Pahl M, Si A, Zhu H, Tautz J, Zhang S (2009) Number-based visual generalisation in the honeybee. PLoS ONE 4:e4263

    PubMed  Article  Google Scholar 

  • Hateren JH, Srinivasan M, Wait P (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 167:649–654

    Article  Google Scholar 

  • Lean G, Shawcross H (2007) Are mobile phones wiping out our bees? News, The Independent [online]. http://newsindependentcouk/environment/wildlife/article2449968ece

  • Li B, Pan B, Han J (2008) Basic terrestrial geomorphological types in China and their circumscriptions. Quat Sci 28:535–543

    Google Scholar 

  • Louveaux J (1969) Ecotype in honey bees. Pro. Int Beekeep Congr Munich 22:499–501

    Google Scholar 

  • McCabe S, Farina W (2009) Odor information transfer in the stingless bee Melipona quadrifasciata: effect of in-hive experiences on classical conditioning of proboscis extension. J Comp Physiol A 195:113–122

    Article  Google Scholar 

  • McCabe S, Farina W (2010) Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). J Comp Physiol A 196:481–490

    Article  CAS  Google Scholar 

  • McCabe S, Hartfelder K, Santana W, Farina W (2007) Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to Africanized honeybees. J Comp Physiol A 193:1089–1099

    Article  CAS  Google Scholar 

  • Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). J Comp Physiol A 56:22–62

    Google Scholar 

  • Menzel R (1968) Das Gedaechtnis der Honigbiene fuer Spektralfarben I.Kurzzeitiges und langzeitiges Behalten. J Comp Physiol A 60:82–102

    Google Scholar 

  • Menzel R (1990) Learning, memory, and “cognition” in honey bees. In: Kesner RP, Olton DS (eds) Neurobiology of comparative cognition. Lawrence Erlbaum Associated, Hillsdale, pp 237–292

    Google Scholar 

  • Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62

    PubMed  Article  CAS  Google Scholar 

  • Menzel R, Geiger K, Chittka L, Joerges J, Kunze J, Uuml U (1996) The knowledge base of bee navigation. J Exp Biol 199:141–146

    PubMed  Google Scholar 

  • Oldroyd BP (2007) What’s killing American honey bees? PLoS Biol 5:e168

    PubMed  Article  Google Scholar 

  • Pahl M, Zhu H, Pix W, Tautz J, Zhang S (2007) Circadian timed episodic-like memory—a bee knows what to do when, and also where. J Exp Biol 210:3559

    PubMed  Article  Google Scholar 

  • Pahl M, Zhu H, Tautz J, Zhang S (2011) Large scale homing in honeybees. PLoS ONE 6:e19669

    PubMed  Article  CAS  Google Scholar 

  • Ruttner F (1975) Races of bees. In: The Hive and the Honey Bee. Dadant and Sons, Hamilton, pp 19–38

  • Srinivasan M, Lehrer M (1988) Spatial acuity of honeybee vision and its spectral properties. J Comp Physiol A 162:159–172

    Article  Google Scholar 

  • Srinivasan M, Zhang S, Witney K (1994) Visual discrimination of pattern orientation by honeybees: performance and implications for cortical’ processing. Proc R Soc Lond Ser B 343:199–210

    Google Scholar 

  • Su S, Cai F, Si A, Zhang S, Tautz J, Chen S (2008) East Learns from West: asiatic honeybees can understand dance language of European honeybees. PLoS ONE 3:e2365

    PubMed  Article  Google Scholar 

  • van Engelsdorp D, Underwood R, Caron D, Hayes J Jr (2007) An estimate of managed colony losses in the winter of 2006–2007: a report commissioned by the apiary inspectors of America. Am Bee J 147:599–603

    Google Scholar 

  • Vorobyev M, Menzel R (1999) Flower advertisement for invertebrates: bees. In: Acher SN et al (eds) The Ecology of Vision. Kluwer Academic Publishers, Dordrecht, pp 537–553

    Google Scholar 

  • Zeng Z (2009) Apiculture. China Agriculture Press, Beijing

    Google Scholar 

  • Zeng Y, Zeng Z, Yan W, Wu X (2010) Effects of three aliphatic esters of brood pheromone on worker feeding and capping behavior and queen development of A. cerana cerana and A. mellifera ligustica. Acta Entomol Sin 53:154–159

    CAS  Google Scholar 

  • Zhang S, Srinivasan M (1994) Prior experience enhances pattern discrimination in insect vision. Nature 368:330–332

    Article  Google Scholar 

  • Zhang S, Srinivasan M, Horridge G (1992) Pattern recognition in honeybees: local and global analysis. Proc R Soc Lond Ser B 248:55

    Article  Google Scholar 

  • Zhang S, Srinivasan M, Collett T (1995) Convergent processing in honeybee vision: multiple channels for the recognition of shape. Proc Natl Acad Sci 92:3029

    PubMed  Article  CAS  Google Scholar 

  • Zhang S, Bartsch K, Srinivasan M (1996) Maze learning by honeybees. Neurobiol Learn Mem 66:267–282

    PubMed  Article  CAS  Google Scholar 

  • Zhang S, Lehrer M, Srinivasan M (1999) Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiol Learn Mem 72:180–201

    PubMed  Article  CAS  Google Scholar 

  • Zhang S, Mizutani A, Srinivasan M (2000) Maze navigation by honeybees: learning path regularity. Learn Memory 7:364–374

    Article  Google Scholar 

  • Zhang S, Srinivasan M, Zhu H, Wong J (2004) Grouping of visual objects by honeybees. J Exp Biol 207:3289

    PubMed  Article  Google Scholar 

  • Zhang S, Bock F, Si A, Tautz J, Srinivasan M (2005) Visual working memory in decision making by honey bees. Proc Natl Acad Sci 102:5250

    PubMed  Article  CAS  Google Scholar 

  • Zhang S, Schwarz S, Pahl M, Zhu H, Tautz J (2006) Honeybee memory: a honeybee knows what to do and when. J Exp Biol 209:4420

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We thank Hong Zhu for invaluable guidance and assistance with all of the experiments, Fei Zhang and Junfeng Liu for help with beekeeping, Jianjin Zeng for constructing the maze apparatus, Haiyan Gan and Xu Han for help with behavioral experiments, Dr. Aung Si and Dr. Zilong Wang for helpful suggestions that improved the manuscript, and theCenter of Analysis and Measurement of Zhejiang University for measuring the spectra of color patterns. This work was supported by the Earmarked Fund for the China Agricultural Research System (no. CARS-45-KXJ12) and the National Natural Science Foundation of China (no. 31060327).

Author information

Affiliations

  1. Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, 330045, People’s Republic of China

    Qiu-Hong Qin, Xu-Jiang He, Liu-Qing Tian & Zhi-Jiang Zeng

  2. ARC Center of Excellence in Vision Science, Research School of Biology, The Australian National University, Canberra, ACT, 0200, Australia

    Shao-Wu Zhang

Authors
  1. Qiu-Hong Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xu-Jiang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liu-Qing Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shao-Wu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhi-Jiang Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shao-Wu Zhang or Zhi-Jiang Zeng.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Qin, QH., He, XJ., Tian, LQ. et al. Comparison of learning and memory of Apis cerana and Apis mellifera . J Comp Physiol A 198, 777–786 (2012). https://doi.org/10.1007/s00359-012-0747-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-012-0747-9

Keywords

  • Apis cerana
  • Apis mellifera
  • Learning and memory
  • Color
  • Grating