Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis

Abstract

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4–5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5a–k
Fig. 6a–d
Fig. 7a, b
Fig. 8a–h
Fig. 9
Fig. 10

References

  1. Amiet F, Herrmann M, Müller A, Neumeyer R (2001) Fauna Helvetica. Apidae 3: Halictus, Lasioglossum. Schweizer Entomologische Gesellschaft, Neuchâtel

    Google Scholar 

  2. Arneson LC, Wcislo WT (2003) Dominant-subordinate relationships in a facultatively social, nocturnal bee, Megalopta genalis (Hymenoptera: Halictidae). J Kansas Entomol Soc 76:183–193

    Google Scholar 

  3. Autrum H (1981) Light and dark adaptation in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol 7/6C. Comparative physiology and evolution of vision in invertebrates. Springer, Berlin Heidelberg New York, pp 1–91

  4. Brännström P (1999) Visual ecology of insect superposition eyes. PhD Thesis, Lund University

  5. Bruno MS, Barnes SM, Goldsmith TH (1977) The visual pigment and the visual cycle of the lobster Homarus. J Comp Physiol 120:123–142

    CAS  Google Scholar 

  6. Dyer FC (1985) Nocturnal orientation by the Asian honey bee, Apis dorsata. Anim Behav 33:769–774

    Google Scholar 

  7. Engel MS (2000) Classification of the bee tribe Augochlorini (Hymenoptera: Halictidae). Bull Am Mus Nat Hist 250:1–90

    Article  Google Scholar 

  8. Fletcher DJC (1978) The African bee, Apis mellifera adansonii, in Africa. Annu Rev Entomol 23:151–171

    Article  Google Scholar 

  9. Hopkins MJG, Fortune Hopkins HC, Sothers CA (2000) Nocturnal pollination of Parkia velutina by Megalopta bees in Amazonia and its possible significance in the evolution of chiropterophily. J Trop Ecol 16:733–746

    Article  Google Scholar 

  10. Horridge GA, Barnard PBT (1965) Movement of palisade in locust retinula cells when illuminated. Q J Micr Sci 106:131–135

    CAS  Google Scholar 

  11. Jander U, Jander R (2002) Allometry and resolution of bee eyes (Apoidea). Arthropod Struct Dev 30:179–193

    Google Scholar 

  12. Janzen DH (1968) Notes on nesting and foraging behavior of Megalopta (Hymenoptera: Halictidae) in Costa Rica. J Kansas Entomol Soc 41:342–350

    Google Scholar 

  13. Kerfoot WB (1967) The lunar periodicity of Sphecodogastra texana, a nocturnal bee (Hymenoptera: Halictidae). Anim Behav 15:479–486

    Google Scholar 

  14. Kirschfeld K (1974) The absolute sensitivity of lens and compound eyes. Z Naturforsch 29C:592–596

    CAS  Google Scholar 

  15. Kolb G, Autrum H (1972) Die Feinstruktur im Auge der Biene bei Hell- und Dunkeladaptation. J Comp Physiol 77:113–125

    Google Scholar 

  16. Kolb G, Autrum H (1974) Selektive Adaptation und Pigmentwanderung in den Sehzellen des Bienenauges. J Comp Physiol 94:1–6

    Google Scholar 

  17. Land MF (1981) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol 7/6B. Vision in invertebrates. Springer, Berlin Heidelberg New York, pp 471–592

  18. Land MF, Eckert H (1985) Maps of the acute zones of fly eyes. J Comp Physiol 156:525–538

    Google Scholar 

  19. Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, New York

  20. Land MF, Osorio DC (1990) Waveguide modes and pupil action in the eyes of butterflies. Proc R Soc Lond B Biol Sci 241:93–100

    Google Scholar 

  21. Land MF, Gibson G, Horwood J (1997) Mosquito eye design: conical rhabdoms are matched to wide aperture lenses. Proc R Soc Lond B Biol Sci 264:1183–1187

    Article  Google Scholar 

  22. Land MF, Gibson G, Horwood J, Zeil J (1999) Fundamental differences in the optical structure of the eyes of nocturnal and diurnal mosquitoes. J Comp Physiol A 185:91–103

    Google Scholar 

  23. Leigh EG Jr (1999) Tropical forest ecology: a view from Barro Colorado Island. Oxford University Press, Oxford

    Google Scholar 

  24. Linsley EG, Cazier MA (1970) Some competitive relationships among matinal and late afternoon foraging activities of caupolicanine bees in southerneastern Arizona (Hymenoptera, Colletidae). J Kansas Entomol Soc 43:251–261

    Google Scholar 

  25. Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore, MD

  26. Miller WH (1981) Ocular optical filtering. In: Autrum H (ed) Handbook of sensory physiology, vol 7/6A. Invertebrate photoreceptors. Springer, Berlin Heidelberg New York, pp 69–143

  27. Miller WH, Møller AR, Bernhard CG (1966) The corneal nipple array. In: Bernard CG (ed) The functional organisation of the compound eye. Pergamon Press, Oxford, pp 21–33

  28. Nilsson D-E (1989) Optics and evolution of the compound eye. In: Stavenga DG, Hardie R (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 30–73

  29. Nilsson D-E, Nilsson HL (1981) A crustacean compound eye adapted for low light intensities (Isopoda). J Comp Physiol 143:503–510

    Google Scholar 

  30. Nilsson D-E, Land MF, Howard J (1988) Optics of the butterfly eye. J Comp Physiol A 162:341–366

    Google Scholar 

  31. Praagh JP van, Ribi WA, Wehrhahn C, Wittmann D (1980) Drone bees fixate the queen with the dorsal frontal part of their compound eyes. J Comp Physiol 136:263–266

    Google Scholar 

  32. Ribi WA (1976) A Golgi-electron microscope method for insect nervous tissue. Stain Technol 51:13–16

    CAS  PubMed  Google Scholar 

  33. Ribi WA (1978) A unique hymenopteran compound eye. The retina fine structure of the digger wasp Sphex cognatus Smith (Hymenoptera, Shecidae). Zool Jb Anat 100:299–342

    Google Scholar 

  34. Ribi WA (1980) The phenomenon of eye glow. Endeavour 5:2–8

    Google Scholar 

  35. Ribi WA (1987) The structural basis of information processing in the visual system of the bee. In: Menzel R, Mercer A (eds) Neurobiology and behavior of honeybees. Springer, Berlin Heidelberg New York, pp 130–140

  36. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge

  37. Roulston TH (1997) Hourly capture of two species of Megalopta (Hymenoptera: Apoidae; Halictidae) at black lights in Panama with notes on nocturnal foraging by bees. J Kansas Entomol Soc 70:189–196

    Google Scholar 

  38. 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 188:1–12

    Article  Google Scholar 

  39. Sakagami SF (1964) Wiederentdeckung des Nestes einer Nachtfurchenbiene, Megalopta sp. am Amazonas (Hymenoptera, Halictidae). Kontyû 32:457–463

  40. Shelly TE, Villalobos EM, Buchman SL, Cane JH (1993) Temporal patterns of floral visitation for two bee species foraging on Solanum. J Kansas Entomol Soc 66:319–327

    Google Scholar 

  41. Smith AR, Wcislo WT, O’Donnel S (2003) Assured fitness returns favor sociality in a mass-provisioning sweat bee Megalopta genalis. Behav Ecol Sociobiol 54:14–21

    Article  Google Scholar 

  42. Stavenga DG (1979) Pseudopupils of compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol 7/6A. Invertebrate photoreceptors. Springer, Berlin Heidelberg New York, pp 357–440

  43. Stavenga DG (2003a) Angular and spectral sensitivity of fly receptors. I. Integrated facet lens and rhabdomere optics. J Comp Physiol A 189:1–17

    CAS  Google Scholar 

  44. Stavenga DG (2003b) Angular and spectral sensitivity of fly receptors. II. Dependence on facet lens F-number and rhabdomere type in Drosophila. J Comp Physiol A 189:189–202

    CAS  Google Scholar 

  45. Stavenga DG, Kuiper JW (1977) Insect pupil mechanisms. I. On the pigment migration in the retinula cells of Hymenoptera (suborder Apocrita). J Comp Physiol A 113:55–72

    Google Scholar 

  46. Warrant EJ (1999) Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vision Res 39:1611–1630

    Article  CAS  PubMed  Google Scholar 

  47. Warrant EJ (2001) The design of compound eyes and the illumination of natural habitats. In: Barth FG, Schmid A (eds) Ecology of sensing. Springer, Berlin Heidelberg New York, pp 187–213

  48. Warrant EJ, McIntyre PD (1991) Strategies for retinal design in arthropod eyes of low F-number. J Comp Physiol A 168:499–512

    Google Scholar 

  49. Warrant EJ, McIntyre PD (1993) Arthropod eye design and the physical limits to spatial resolving power. Prog Neurobiol 40:413–461

    CAS  PubMed  Google Scholar 

  50. Warrant EJ, Nilsson D-E (1998) Absorption of white light in photoreceptors. Vision Res 38:195–207

    CAS  PubMed  Google Scholar 

  51. Warrant E, Porombka T, Kirchner WH (1996) Neural image enhancement allows honeybees to see at night. Proc R Soc Lond B Biol Sci 263:1521–1526

    Google Scholar 

  52. Wolda H, Roubik DW (1986) Nocturnal bee abundance and seasonal bee activity in a Panamanian forest. Ecology 67:426–433

    Google Scholar 

Download references

Acknowledgements

We would like to thank Almut Kelber, Doekele Stavenga, Mark Holdstock and the two anonymous referees for critically reading the manuscript, Ladina Ribi for the taxonomic drawing of Megalopta, Rita Wallén and Carin Rasmussen for histological and technical support, Rikard Frederiksen for help with the corneal replicas, Mikael Sörenson and Jan Tengö for taxonomical help, as well as Victor Gonzales and Sara Juhl for help with fieldwork. We thank William T. Wcislo and the staff of the Smithsonian Tropical Research Institute, Panama City, for their help and the Autoridad Nacional del Ambiente of the Republic of Panama for permission to export bees. The histological work was partly done at the Center for Visual Sciences, Research School of Biological Science, Australian National University, Canberra.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Birgit Greiner.

Additional information

B.G. is thankful for travel awards from the Royal Physiographic Society, the Per Westlings Fond, the Foundation of Dagny and Eilert Ekvall and the Royal Swedish Academy of Sciences. E.J.W. is grateful for the support of a Smithsonian Short-Term Research Fellowship, the Swedish Research Council, the Crafoord Foundation, the Wenner-Gren Foundation and the Royal Physiographic Society of Lund for their ongoing support

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Greiner, B., Ribi, W.A. & Warrant, E.J. Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis . Cell Tissue Res 316, 377–390 (2004). https://doi.org/10.1007/s00441-004-0883-9

Download citation

Keywords

  • Visual system
  • Nocturnal vision
  • Apposition compound eye
  • Retina structure
  • Dim light
  • Megalopta genalis (Insecta)