Journal of Comparative Physiology A

, Volume 195, Issue 6, pp 571–583 | Cite as

Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles

  • Hema SomanathanEmail author
  • Almut Kelber
  • Renee M. Borges
  • Rita Wallén
  • Eric J. Warrant
Original Paper


Most bees are diurnal, with behaviour that is largely visually mediated, but several groups have made evolutionary shifts to nocturnality, despite having apposition compound eyes unsuited to vision in dim light. We compared the anatomy and optics of the apposition eyes and the ocelli of the nocturnal carpenter bee, Xylocopa tranquebarica, with two sympatric species, the strictly diurnal X. leucothorax and the occasionally crepuscular X. tenuiscapa. The ocelli of the nocturnal X. tranquebarica are unusually large (diameter ca. 1 mm) and poorly focussed. Moreover, their apposition eyes show specific visual adaptations for vision in dim light, including large size, large facets and very wide rhabdoms, which together make these eyes 9 times more sensitive than those of X. tenuiscapa and 27 times more sensitive than those of X. leucothorax. These differences in optical sensitivity are surprisingly small considering that X. tranquebarica can fly on moonless nights when background luminance is as low as 10−5 cd m−2, implying that this bee must employ additional visual strategies to forage and find its way back to the nest. These strategies may include photoreceptors with longer integration times and higher contrast gains as well as higher neural summation mechanisms for increasing visual reliability in dim light.


Apposition compound eyes Bees Ocelli Optical sensitivity Xylocopa 



We wish to thank Kalu Kurade, Ganpat Lohakare, Subhash Vangere, Narayan Chikhale and Vittal Lohakare for help with field work, Carina Rasmussen and Eva Landgren for patient assistance with the eye maps and Fredrik Jönsson for help with focal length measurements. We are thankful to the Forest Department of Maharashtra State for research permissions. We are extremely grateful to Charles Michener for species determination. This research was supported by grants from the Swedish International Development Agency (SIDA) to AK and RMB and from the Swedish Research Council (VR) to EJW and AK, and a Wenner-Gren Foundation post-doctoral fellowship to HS. We declare that the experiments comply with the “Principles of animal care” and also with the current laws of the countries in which the experiments were performed.


  1. Blest AD, Land MF (1977) The physiological optics of Dinopis subrufus L. Koch: a fish-lens in a spider. Proc R Soc Lond B 196:197–222PubMedCrossRefGoogle Scholar
  2. Frederiksen R, Warrant EJ (2008) Visual sensitivity in the crepuscular owl butterfly Caligo memnon and the diurnal blue morpho, Morpho peleides: a clue to explain the evolution of nocturnal apposition eyes? J Exp Biol 211:844–851PubMedCrossRefGoogle Scholar
  3. Frederiksen R, Wcislo WT, Warrant EJ (2008) Visual reliability and information rate in the retina of a nocturnal bee. Curr Biol 18:349–353PubMedCrossRefGoogle Scholar
  4. Greiner B (2006) Visual adaptations in the night-active wasp Apoica pallens. J Comp Neurol 495:255–262PubMedCrossRefGoogle Scholar
  5. Greiner B, Ribi WA, Warrant EJ (2004) Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis. Cell Tissue Res 316:377–390PubMedCrossRefGoogle Scholar
  6. Greiner B, Narendra A, Reid SF, Dacke M, Ribi WA, Zeil J (2007) Eye structure correlates with distinct foraging bout timing in primitive ants. Curr Biol 17:R879–R880PubMedCrossRefGoogle Scholar
  7. Greiner B, Cronin TW, Ribi WA, Wcislo WT, Warrant EJ (2008) Polarisation vision in the nocturnal bee Megalopta genalis and its possible role in homing. J Comp Physiol A 193:591–600CrossRefGoogle Scholar
  8. Homann H (1924) Zum Problem der Ocellenfunktion bei den Insekten. Zeitschr vergl Physiol 1:541–578CrossRefGoogle Scholar
  9. Horridge GA (1978) Separation of visual axes in apposition compound eyes. Phil Trans R Soc Lond B Biol Sci 285:1–59CrossRefGoogle Scholar
  10. Jander U, Jander R (2002) Allometry and resolution of bee eyes (Apoidea). Arthropod Struct Dev 30:179–193PubMedCrossRefGoogle Scholar
  11. Kelber A, Warrant EJ, Pfaff M, Wallén R, Theobald JC, Wcislo W, Raguso R (2006) Light intensity limits foraging activity in nocturnal and crepuscular bees. Behav Ecol 17:63–72CrossRefGoogle Scholar
  12. Kerfoot WB (1967) Correlation between ocellar size and the foraging activities of bees (Hymenoptera, Apoidea). Am Nat 101:65–70CrossRefGoogle Scholar
  13. Kirschfeld K (1974) The absolute sensitivity of lens and compound eyes. Z Naturforsch C 29:592–596Google Scholar
  14. Land MF (1981) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin, pp 471–592Google Scholar
  15. Land MF (1997) Visual acuity in insects. Ann Rev Entomol 42:147–177CrossRefGoogle Scholar
  16. Land MF, Eckert H (1985) Maps of the acute zones of fly eyes. J Comp Physiol A 156:525–538CrossRefGoogle Scholar
  17. Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, OxfordGoogle Scholar
  18. Land MF, Osorio DC (1990) Waveguide modes and pupil action in the eyes of butterflies. Proc R Soc Lond B 241:93–100CrossRefGoogle Scholar
  19. Menzi U (1987) Visual adaptation in nocturnal and diurnal ants. J Comp Physiol A 160:11–21CrossRefGoogle Scholar
  20. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, CambridgeGoogle Scholar
  21. Rutowski RL, Warrant EJ (2002) Visual field structure in a butterfly Asterocampa leilia (Lepidoptera, Nymphalidae): dimensions and regional variation in acuity. J Comp Physiol A 188:1–12CrossRefGoogle Scholar
  22. Rutowski RL, Gislén L, Warrant EJ (2009) Visual acuity and sensitivity increase allometrically with body size in butterflies. Arthropod Struct Dev 38:91–100PubMedCrossRefGoogle Scholar
  23. Snyder AW (1977) Acuity of compound eyes: physical limitations and design. J Comp Physiol 116:161–182CrossRefGoogle Scholar
  24. Snyder AW (1979) Physics of vision in compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin, pp 225–313Google Scholar
  25. Somanathan H, Borges RM (2001) Nocturnal pollination by the carpenter bee Xylocopa tenuiscapa (Apidae) and the effect of floral display on fruit set of Heterophragma quadriloculare (Bignoniaceae) in India. Biotropica 33:78–89Google Scholar
  26. Somanathan H, Borges RM, Warrant EJ, Kelber A (2008a) Visual ecology of Indian carpenter bees. I. Light intensity and flight activity. J Comp Physiol A 194:97–107CrossRefGoogle Scholar
  27. Somanathan H, Borges RM, Warrant EJ, Kelber A (2008b) Nocturnal bees can learn the colours of landmarks in starlight. Curr Biol 18:349–353CrossRefGoogle Scholar
  28. Srygley RB, Penz CM (1999) Lekking in neotropical owl butterflies, Caligo illioneus and C. oileus (Lepidoptera: Brassolinae). J Insect Behav 12:81–103CrossRefGoogle Scholar
  29. Stavenga DG (2003) Angular and spectral sensitivity of fly photoreceptors. I. Integrated facet lens and rhabdomere optics. J Comp Physiol A 189:1–17Google Scholar
  30. Straw AD, Warrant EJ, O’Carroll DC (2006) A ‘bright zone’ in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity. J Exp Biol 209:4339–4354PubMedCrossRefGoogle Scholar
  31. Theobald JC, Greiner B, Wcislo WT, Warrant EJ (2005) Visual summation in night-flying sweat bees: a theoretical study. Vision Res 46:2298–2309CrossRefGoogle Scholar
  32. van Hateren JH, Hardie RC, Rudolph A, Laughlin SB, Stavenga DG (1989) The bright zone, a specialized dorsal eye region in the male blowfly Chrysomyia megacephala. J Comp Physiol A 164:297–308CrossRefGoogle Scholar
  33. Warrant EJ (1999) Seeing better at night: lifestyle, eye design and the optimal strategy of spatial and temporal summation. Vision Res 33:1011–1017Google Scholar
  34. Warrant EJ (2004) Vision in the dimmest habitats on earth. J Comp Physiol A 190:765–789CrossRefGoogle Scholar
  35. Warrant EJ (2008) Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J Exp Biol 22:1737–1746CrossRefGoogle Scholar
  36. Warrant EJ, Nilsson DE (1998) Absorption of white light in photoreceptors. Vision Res 38:195–207PubMedCrossRefGoogle Scholar
  37. Warrant EJ, Kelber A, Gislen A, Greiner B, Ribi W, Wcislo WT (2004) Nocturnal vision and landmark orientation in a tropical halictid bee. Curr Biol 14:1309–1318PubMedCrossRefGoogle Scholar
  38. Warrant EJ, Kelber A, Wallén R, Wcislo W (2006) Ocellar optics in diurnal and nocturnal bees and wasps. Arthropod Struct Dev 35:293–305PubMedCrossRefGoogle Scholar
  39. Wcislo WT, Arneson L, Roesch K, Gonzalez V, Smith A, Fernández-Marín H (2004) The evolution of nocturnal behavior in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies? Biol J Linn Soc 83:377–387CrossRefGoogle Scholar
  40. Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6C. Springer, Berlin, pp 287–616Google Scholar
  41. Wellington WG (1974) Bumblebee orientation and navigation at dusk. Science 183:550–551PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Hema Somanathan
    • 1
    • 2
    Email author
  • Almut Kelber
    • 1
  • Renee M. Borges
    • 2
  • Rita Wallén
    • 1
  • Eric J. Warrant
    • 1
  1. 1.Department of Cell and Organism Biology, ZoologyLund UniversityLundSweden
  2. 2.Centre for Ecological SciencesIndian Institute of ScienceBangaloreIndia

Personalised recommendations