Abstract
To understand how insect pollinators find flowers against complex backgrounds in diverse natural habitats, it is required to accurately estimate the thresholds for target detection. Detection thresholds for single targets vary between bee species and have been estimated in the Western honeybee, a species of bumblebee and in a stingless bee species. We estimated the angular range of detection for coloured targets in the Asian honeybee Apis cerana. Using a Y-maze experimental set up, we show that targets that provided both chromatic and green receptor contrast were detected at a minimum visual angle of 7.7°, while targets with only chromatic contrast were detected at a minimum angle of 13.2°. Our results thus provide a robust foundation for future studies on the visual ecology of bees in a comparative interspecific framework.
Similar content being viewed by others
References
Autrum H, Zwehl V (1964) Die spektrale Empfindlichkeit einzelner Sehzellen des Bienenauges. Z Vergl Physiol 48:357–384
Balamurali GS, Nicholls E, Somanathan H, Hempel de Ibarra N (2018) A comparative analysis of colour preferences in temperate and tropical social bees. Sci Nat. https://doi.org/10.1007/s00114-017-1531-z
Brandt R, Vorobyev M (1997) Metric analysis of threshold spectral sensitivity in the honeybee. Vision Res 37:425–439. https://doi.org/10.1016/S0042-6989(96)00195-2
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510. https://doi.org/10.1146/annurev.ento.46.1.471
Brito VLG, Weynans K, Sazima M, Lunau K (2015) Trees as huge flowers and flowers as oversized floral guides: the role of floral color change and retention of old flowers in Tibouchina pulchra. Front Plant Sci 6:362. https://doi.org/10.3389/fpls.2015.00362
Cardinal S, Straka J, Danforth BN (2010) Comprehensive phylogeny of Apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proc Natl Acad Sci U S A 107:16207–16211. https://doi.org/10.1073/pnas.1006299107
Chittka L, Spaethe J (2007) Visual search and the importance of time in complex decision making by bees. Arthropod Plant Interact 1:37–44. https://doi.org/10.1007/s11829-007-9001-8
Chittka L, Beier W, Hertel H et al (1992) Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera. J Comp Physiol A 170:545–563. https://doi.org/10.1007/BF00199332
Dornhaus A, Chittka L (2004) Why do honey bees dance? Behav Ecol Sociobiol 55:395–401. https://doi.org/10.1007/s00265-003-0726-9
Dyer FC (1985) Nocturnal orientation by the Asian honey bee, Apis dorsata. Anim Behav 33:769–774
Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194:617
Dyer AG, Streinzer M, Garcia J (2016) Flower detection and acuity of the Australian native stingless bee Tetragonula carbonaria Sm. J Comp Physiol Neuroethol Sensory Neural Behav Physiol 202:629–639. https://doi.org/10.1007/s00359-016-1107-y
Farnier K, Dyer AG, Taylor GS et al (2015) Visual acuity trade-offs and microhabitat-driven adaptation of searching behaviour in psyllids (Hemiptera: Psylloidea: Aphalaridae). J Exp Biol 218:1564–1571. https://doi.org/10.1242/jeb.120808
Giurfa M, Vorobyev M (1998) The angular range of achromatic target detection by honey bees. J Comp Physiol Sensory Neural Behav Physiol 183:101–110. https://doi.org/10.1007/s003590050238
Giurfa M, Vorobyev M, Kevan P, Menzel R (1996) Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J Comp Physiol A 178:699–709. https://doi.org/10.1007/BF00227381
Giurfa M, Vorobyev M, Brandt R et al (1997) Discrimination of coloured stimuli by honeybees: Alternative use of achromatic and chromatic signals. J Comp Physiol Sensory Neural Behav Physiol 180:235–243. https://doi.org/10.1007/s003590050044
Greiner B, Ribi WA, Warrant EJ (2004) Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis. Cell Tissue Res 316:377–390
Heinrich B (2004) Bumblebee economics. Harvard University Press, Cambridge
Hempel De Ibarra N, Vorobyev M, Brandt R, Giurfa M (2000) Detection of bright and dim colours by honeybees. J Exp Biol 203:3289–3298
Hempel de Ibarra N, Vorobyev M, Menzel R (2014) Mechanisms, functions and ecology of colour vision in the honeybee. J Comp Physiol Neuroethol Sensory Neural Behav Physiol 200:411–433. https://doi.org/10.1007/s00359-014-0915-1
Hempel de Ibarra N, Langridge KV, Vorobyev M (2015) More than colour attraction: behavioural functions of flower patterns. Curr Opin Insect Sci 12:64–70. https://doi.org/10.1016/j.cois.2015.09.005
Kaiser W (1974) The spectral sensitivity of the honeybee’s optomotor walking response. J Comp Physiol 90:405–408. https://doi.org/10.1007/BF00694179
Kaiser W, Liske E (1974) Die optomotorischen Reaktionen von fixiert fliegenden Bienen bei Reizung mit Spektrallichtern. J Comp Physiol 89:391–408. https://doi.org/10.1007/BF00695355
Kapustjanskij A, Streinzer M, Paulus HF, Spaethe J (2007) Bigger is better: Implications of body size for flight ability under different light conditions and the evolution of alloethism in bumblebees. Funct Ecol 21:1130–1136. https://doi.org/10.1111/j.1365-2435.2007.01329.x
Kapustjansky A, Chittka L, Spaethe J (2010) Bees use three-dimensional information to improve target detection. Naturwissenschaften 97:229–233. https://doi.org/10.1007/s00114-009-0627-5
Kelber A, Somanathan H (2019) Spatial vision and visually guided behavior in Apidae. Insects 10:1–17. https://doi.org/10.3390/insects10120418
Kevan PG (1972) Insect pollination of high Arctic flowers. J Ecol 60:831. https://doi.org/10.2307/2258569
Kunze J, Gumbert A (2001) The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behav Ecol 12:447–456. https://doi.org/10.1093/beheco/12.4.447
Land MF (1997) Visual acuity in insects. Annu Rev Entomol 42:147–177. https://doi.org/10.1146/annurev.ento.42.1.147
Land MF, Nilsson D-E (2012) Animal eyes. Oxford University Press, Oxford
Lehrer M, Srinivasan MV (1994) Active vision in honeybees: Task-oriented suppression of an innate behaviour. Vision Res 34:511–516. https://doi.org/10.1016/0042-6989(94)90164-3
Lehrer M, Horridge GA, Zhang SW, Gadagkar R (1995) Shape vision in bees: innate preference for flower-like patterns. Phil Trans R Soc B Biol Sci 347:123–137. https://doi.org/10.1098/rstb.1995.0017
Leonard AS, Masek P (2014) Multisensory integration of colors and scents: Insights from bees and flowers. J Comp Physiol Neuroethol Sensory Neural Behav Physiol 200:463–474. https://doi.org/10.1007/s00359-014-0904-4
Lichtenstein L, Brockmann A, Spaethe J (2019) Learning of monochromatic stimuli in Apis cerana and Apis mellifera by means of PER conditioning. J Insect Physiol 114:30–34. https://doi.org/10.1016/j.jinsphys.2019.02.006
Menzel R (1985) Learning in honey bees in an ecological and behavioral context. Fortschritte Der Zoologie (Stuttgart) 31:55–74
Menzel R, Backhaus W (1991) Colour vision in insects. In: Gouras P (ed) Vision and visual disfunction. Macmillan, London, pp 262–288
Niggebrügge C, Hempel De Ibarra N (2003) Colour-dependent target detection by bees. J Comp Physiol Neuroethol Sensory Neural Behav Physiol 189:915–918. https://doi.org/10.1007/s00359-003-0466-3
Peitsch D, Fietz A, Hertel H et al (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170:23–40
Price RIA, Grüter C (2015) Why, when and where did honey bee dance communication evolve? Front Ecol Evol 3:1–7. https://doi.org/10.3389/fevo.2015.00125
Qin QH, He XJ, Tian LQ et al (2012) Comparison of learning and memory of Apis cerana and Apis mellifera. J Comp Physiol Neuroethol Sensory Neural Behav Physiol 198:777–786. https://doi.org/10.1007/s00359-012-0747-9
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Renoult JP, Kelber A, Schaefer HM (2017) Colour spaces in ecology and evolutionary biology. Biol Rev 92:292–315. https://doi.org/10.1111/brv.12230
Rodríguez I, Gumbert A, De Ibarra NH et al (2004) Symmetry is in the eye of the “beeholder”: Innate preference for bilateral symmetry in flower-naïve bumblebees. Naturwissenschaften 91:374–377. https://doi.org/10.1007/s00114-004-0537-5
Sayed Mehdi E, Vaziritabar Shakib C (2016) Comparison olfactory learning three races of bees (Apis mellifera meda, Apis mellifera carnica and Apis cerana F.) under laboratory conditions and memory recall in drones of hive honeybee species in Iran. J Entomol Zool Stud JEZS 4:1046–1059
Seeley TD, Visscher PK (1988) Assessing the benefits of cooperation in honeybee foraging: search costs, forage quality, and competitive ability. Behav Ecol Sociobiol 22:229–237. https://doi.org/10.1007/BF00299837
Somanathan H, Borges RM, Warrant EJ, Kelber A (2008) Visual ecology of Indian carpenter bees I: Light intensities and flight activity. J Comp Physiol Neuroethol Sensory Neural, Behav Physiol 194:97–107. https://doi.org/10.1007/s00359-007-0291-1
Somanathan H, Warrant EJ, Borges RM et al (2009a) Resolution and sensitivity of the eyes of the Asian honeybees Apis florea, Apis cerana and Apis dorsata. J Exp Biol 212:2448–2453. https://doi.org/10.1242/jeb.031484
Somanathan H, Kelber A, Borges RM et al (2009b) Visual ecology of Indian carpenter bees II: Adaptations of eyes and ocelli to nocturnal and diurnal lifestyles. J Comp Physiol Neuroethol Sensory Neural, Behav Physiol 195:571–583. https://doi.org/10.1007/s00359-009-0432-9
Spaethe J, Chittka L (2003) Interindividual variation of eye optics and single object resolution in bumblebees. J Exp Biol 206:3447–3453. https://doi.org/10.1242/jeb.00570
Spaethe J, Streinzer M, Eckert J et al (2014) Behavioural evidence of colour vision in free flying stingless bees. J Comp Physiol Neuroethol Sensory Neural, Behav Physiol 200:485–496. https://doi.org/10.1007/s00359-014-0886-2
Srinivasan MV, Lehrer M (1984) Temporal acuity of honeybee vision: behavioural studies using moving stimuli. J Comp Physiol Neuroethol Sensory Neural Behav Physiol 155:297–312. https://doi.org/10.1007/BF00610583
Streinzer M, Brockmann A, Nagaraja N, Spaethe J (2013) Sex and caste-specific variation in compound eye morphology of five honeybee species. PLoS ONE 8:1–9. https://doi.org/10.1371/journal.pone.0057702
Von Frisch K (1914) Der Farbensinn und Formensinn der Biene. Zool Jahrb Allg Zool 37:1–187
Von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge
Vorobyev M, Brandt R, Peitsch D et al (2001) Colour thresholds and receptor noise: Behaviour and physiology compared. Vision Res 41:639–653. https://doi.org/10.1016/S0042-6989(00)00288-1
Wertlen AM, Niggebrügge C, Vorobyev M, Hempel De Ibarra N (2008) Detection of patches of coloured discs by bees. J Exp Biol 211:2101–2104. https://doi.org/10.1242/jeb.014571
Acknowledgements
BGS and HS conceptualised the study, wrote and revised the manuscript. AM and AMVK conducted experiments and collected the data under the supervision of BGS and HS. BGS conducted the pilot experiments, and analysed the data. HS acknowledges funding from Indian Institute of Science Education and Research Thiruvananthapuram (IISER TVM). AM was supported by an internship from Indian Institute of Science Education and Research Thiruvananthapuram (IISER-TVM). We thank Asmi Jezeera and Sajesh Vijayan for critical discussions and suggestions on a previous version of the manuscript. We also thank the two anonymous reviewers for their constructive comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Meena, A., Kumar, A.M.V., Balamurali, G.S. et al. Visual detection thresholds in the Asian honeybee, Apis cerana. J Comp Physiol A 207, 553–560 (2021). https://doi.org/10.1007/s00359-021-01496-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-021-01496-0