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

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Abstract

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.

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References

  • Blest AD, Land MF (1977) The physiological optics of Dinopis subrufus L. Koch: a fish-lens in a spider. Proc R Soc Lond B 196:197–222

    Article  PubMed  CAS  Google Scholar 

  • 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 211:844–851

    Article  PubMed  Google Scholar 

  • Frederiksen R, Wcislo WT, Warrant EJ (2008) Visual reliability and information rate in the retina of a nocturnal bee. Curr Biol 18:349–353

    Article  PubMed  CAS  Google Scholar 

  • Greiner B (2006) Visual adaptations in the night-active wasp Apoica pallens. J Comp Neurol 495:255–262

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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–R880

    Article  PubMed  CAS  Google Scholar 

  • 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 193:591–600

    Article  Google Scholar 

  • Homann H (1924) Zum Problem der Ocellenfunktion bei den Insekten. Zeitschr vergl Physiol 1:541–578

    Article  Google Scholar 

  • Horridge GA (1978) Separation of visual axes in apposition compound eyes. Phil Trans R Soc Lond B Biol Sci 285:1–59

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 17:63–72

    Article  Google Scholar 

  • Kerfoot WB (1967) Correlation between ocellar size and the foraging activities of bees (Hymenoptera, Apoidea). Am Nat 101:65–70

    Article  Google Scholar 

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

    Google Scholar 

  • Land MF (1981) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin, pp 471–592

    Google Scholar 

  • Land MF (1997) Visual acuity in insects. Ann Rev Entomol 42:147–177

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Menzi U (1987) Visual adaptation in nocturnal and diurnal ants. J Comp Physiol A 160:11–21

    Article  Google Scholar 

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

    Google Scholar 

  • 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 

  • Rutowski RL, Gislén L, Warrant EJ (2009) Visual acuity and sensitivity increase allometrically with body size in butterflies. Arthropod Struct Dev 38:91–100

    Article  PubMed  CAS  Google Scholar 

  • Snyder AW (1977) Acuity of compound eyes: physical limitations and design. J Comp Physiol 116:161–182

    Article  Google Scholar 

  • Snyder AW (1979) Physics of vision in compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin, pp 225–313

    Google Scholar 

  • 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 33:78–89

    Google Scholar 

  • 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 194:97–107

    Article  Google Scholar 

  • Somanathan H, Borges RM, Warrant EJ, Kelber A (2008b) Nocturnal bees can learn the colours of landmarks in starlight. Curr Biol 18:349–353

    Article  Google Scholar 

  • Srygley RB, Penz CM (1999) Lekking in neotropical owl butterflies, Caligo illioneus and C. oileus (Lepidoptera: Brassolinae). J Insect Behav 12:81–103

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • 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 209:4339–4354

    Article  PubMed  Google Scholar 

  • Theobald JC, Greiner B, Wcislo WT, Warrant EJ (2005) Visual summation in night-flying sweat bees: a theoretical study. Vision Res 46:2298–2309

    Article  Google Scholar 

  • 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 164:297–308

    Article  Google Scholar 

  • Warrant EJ (1999) Seeing better at night: lifestyle, eye design and the optimal strategy of spatial and temporal summation. Vision Res 33:1011–1017

    Google Scholar 

  • Warrant EJ (2004) Vision in the dimmest habitats on earth. J Comp Physiol A 190:765–789

    Article  Google Scholar 

  • Warrant EJ (2008) Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J Exp Biol 22:1737–1746

    Article  Google Scholar 

  • Warrant EJ, Nilsson DE (1998) Absorption of white light in photoreceptors. Vision Res 38:195–207

    Article  PubMed  CAS  Google Scholar 

  • 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 14:1309–1318

    Article  PubMed  CAS  Google Scholar 

  • Warrant EJ, Kelber A, Wallén R, Wcislo W (2006) Ocellar optics in diurnal and nocturnal bees and wasps. Arthropod Struct Dev 35:293–305

    Article  PubMed  Google Scholar 

  • 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 83:377–387

    Article  Google Scholar 

  • Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6C. Springer, Berlin, pp 287–616

    Google Scholar 

  • Wellington WG (1974) Bumblebee orientation and navigation at dusk. Science 183:550–551

    Article  PubMed  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Cell and Organism Biology, Zoology, Lund University, 22363, Lund, Sweden

    Hema Somanathan, Almut Kelber, Rita Wallén & Eric J. Warrant

  2. Centre for Ecological Sciences, Indian Institute of Science, Bangalore, 560012, India

    Hema Somanathan & Renee M. Borges

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  1. Hema Somanathan
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  2. Almut Kelber
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  3. Renee M. Borges
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  4. Rita Wallén
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  5. Eric J. Warrant
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Correspondence to Hema Somanathan.

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Somanathan, H., Kelber, A., Borges, R.M. et al. Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles. J Comp Physiol A 195, 571–583 (2009). https://doi.org/10.1007/s00359-009-0432-9

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  • DOI: https://doi.org/10.1007/s00359-009-0432-9

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