How do birds look at their world? A novel avian visual fixation strategy

  • Shannon R. Butler
  • Jennifer J. Templeton
  • Esteban Fernández-Juricic
Original Article

Abstract

A central assumption in behavioral research is that the observer knows where an animal is looking; however, establishing when an animal is gazing (i.e., visually fixating on an object) has been challenging in species with laterally placed eyes. We quantitatively tested three fixation strategies proposed in the literature for birds, using European starlings (Sturnus vulgaris). We did not find strong support for any of the three strategies, despite high statistical a priori power (93%). However, we did observe a new visual fixation strategy that we labeled monocular alternating fixation. In this strategy, starlings moved their heads to make multiple fixations with a single eye before switching to the other eye and repeating the same process. Additionally, we established that individuals favored using the left over the right eye, supporting that laterality in starlings is left-eye dominant. The newly observed fixation strategy may be associated with the high level of intra-retinal variation (density of photoreceptors, overall sensitivity of visual pigments, etc.) in the starling retina. From a functional perspective, this monocular alternating fixation strategy may be beneficial to integrate the different types of information gathered by the different portions of each retina more quickly. We discuss the implications of our results for designing and interpreting behavioral experiments that require an understanding of where a bird is looking.

Significance statement

This is the first study to quantitatively test three hypotheses in the literature about how animals with laterally placed eyes look at objects. We found that there was not strong support for any of these three strategies, but found support for a newly described strategy for birds to look at objects (i.e., multiple looks with a single eye before switching to the other eye).

Keywords

Vision Laterality European starling Fixation Avian vision 

Notes

Acknowledgements

We would like to thank three anonymous reviewers or their helpful comments. Hannah Smith (HS) was very helpful in collecting the data from the videos. We are grateful to the USDA APHIS in Ohio who provided the starlings for this experiment, as well as Tom Gnoske from the Field Museum of Natural History in Chicago, IL, who graciously prepared and donated one of our Cooper’s hawk models, and Dr. Barney Dunning from the Department of Forestry and Natural Resources at Purdue University for allowing us to borrow another Cooper’s hawk model.

Compliance with ethical standards

Ethical approval

The Institutional Animal Care and Use Committee of Purdue University (protocol 1306000876) approved all animal-handling and care procedures. The state of Ohio does not require a permit to capture European starlings because starlings are an invasive species. There is also no required paperwork to transport European starlings from Ohio to Indiana according to the State and Federal organizations (Ohio Department of Natural Resources: Wildlife; Indiana Department of Natural Resources: Fish and Wildlife; Unites States Department of Agriculture, APHIS, Wildlife Services). For the experiment in the supplementary material, procedures were approved by the Institutional Animal Care and Use Committee of Franklin & Marshall College (Protocol # 2000-05).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2018_2455_MOESM1_ESM.xlsx (152 kb)
ESM 1 (XLSX 152 kb)
265_2018_2455_MOESM2_ESM.mp4 (206 kb)
Video 1 (MP4 206 kb)
265_2018_2455_MOESM3_ESM.mp4 (218 kb)
Video 2 (MP4 218 kb)
265_2018_2455_MOESM4_ESM.mp4 (231 kb)
Video 3 (MP4 230 kb)
265_2018_2455_MOESM5_ESM.docx (19 kb)
ESM 2 (DOCX 19 kb)

References

  1. Beauchamp G (2013) Foraging success in a wild species of bird varies depending on which eye is used for anti-predator vigilance. Laterality 18(2):194–202.  https://doi.org/10.1080/1357650X.2011.648194 CrossRefPubMedGoogle Scholar
  2. Bloch S, Martinoya C (1982) Comparing frontal and lateral viewing in the pigeon. I. Tachistoscopic visual acuity as a function of distance. Behav Brain Res 5(3):231–244.  https://doi.org/10.1016/0166-4328(82)90031-6 CrossRefPubMedGoogle Scholar
  3. Butler SR, Fernández-Juricic E (2014) European starlings recognize the location of robotic conspecific attention. Biol Lett 10(10):20140665.  https://doi.org/10.1098/rsbl.2014.0665 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Butler SR, Fernández-Juricic E (2018) European starlings use their acute vision to check on feline predators but not on conspecifics. PLoS ONE 13(1):e0188857.  https://doi.org/10.1371/journal.pone.0188857 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Butler SR, Hosinski EC, Lucas JR, Fernández-Juricic E (2016) Social birds copy each other’s lateral scans while monitoring group mates with low-acuity vision. Anim Behav 121:21–31.  https://doi.org/10.1016/j.anbehav.2016.08.002 CrossRefGoogle Scholar
  6. Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Earlbaum Associates, HilsdaleGoogle Scholar
  7. Davidson GL, Butler S, Fernández-Juricic E, Thornton A, Clayton NS (2014) Gaze sensitivity: function and mechanisms from sensory and cognitive perspectives. Anim Behav 87:3–15.  https://doi.org/10.1016/j.anbehav.2013.10.024 CrossRefGoogle Scholar
  8. Dawkins M (2002) What are birds looking at? Head movements and eye use in chickens. Anim Behav 63(5):991–998.  https://doi.org/10.1006/anbe.2002.1999 CrossRefGoogle Scholar
  9. Dawkins MS (1995) How do hens view other hens ? The use of lateral and binocular visual fields in social recognition. Behaviour 132(7):591–606.  https://doi.org/10.1163/156853995X00225 CrossRefGoogle Scholar
  10. Diedrich E, Schaeffel F (2009) Spatial resolution, contrast sensitivity, and sensitivity to defocus of chicken retinal ganglion cells in vitro. Vis Neurosci 26(5-6):467–476.  https://doi.org/10.1017/S0952523809990253 CrossRefPubMedGoogle Scholar
  11. Dolan T, Fernández-Juricic E (2010) Retinal ganglion cell topography of five species of ground-foraging birds. Brain Behav Evol 75(2):111–121.  https://doi.org/10.1159/000305025 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fernández-Juricic E (2012) Sensory basis of vigilance behavior in birds: synthesis and future prospects. Behav Process 89(2):143–152.  https://doi.org/10.1016/j.beproc.2011.10.006 CrossRefGoogle Scholar
  13. Fernández-Juricic E, Erichsen JT, Kacelnik A (2004) Visual perception and social foraging in birds. Trends Ecol Evol 19:25–31.  https://doi.org/10.1016/j.tree.2003.10.003 CrossRefPubMedGoogle Scholar
  14. Fernández-Juricic E, Ojeda A, Deisher M, Burry B, Baumhardt P, Stark A, Elmore AG, Ensminger AL (2013) Do male and female cowbirds see their world differently? Implications for sex differences in the sensory system of an avian brood parasite. PLoS One 8(3):e58985.  https://doi.org/10.1371/journal.pone.0058985 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Fernández-Juricic E, Tran E (2007) Changes in vigilance and foraging behaviour with light intensity and their effects on food intake and predator detection in house finches. Anim Behav 74(5):1381–1390.  https://doi.org/10.1016/j.anbehav.2007.01.005 CrossRefGoogle Scholar
  16. Forsman A, Appelqvist S (1998) Visual predators impose correlational selection on prey color pattern and behavior. Behav Ecol 9(4):409–413Google Scholar
  17. Franklin WE, Lima SL (2001) Laterality in avian vigilance: do sparrows have a favourite eye? Anim Behav 62(5):879–885.  https://doi.org/10.1006/anbe.2001.1826 CrossRefGoogle Scholar
  18. Grodzinski U, Watanabe A, Clayton NS (2012) Peep to pilfer: what scrub-jays like to watch when observing others. Anim Behav 83(5):1253–1260.  https://doi.org/10.1016/j.anbehav.2012.02.018 CrossRefGoogle Scholar
  19. Guo K, Robertson RG, Mahmoodi S, Tadmor Y, Young MP (2003) How do monkeys view faces?--a study of eye movements. Exp Brain Res 150(3):363–374.  https://doi.org/10.1007/s00221-003-1429-1 CrossRefPubMedGoogle Scholar
  20. Hart NS, Partridge JC, Cuthill IC (2000) Retinal asymmetry in birds. Curr Biol 10(2):115–117.  https://doi.org/10.1016/S0960-9822(00)00297-9 CrossRefPubMedGoogle Scholar
  21. Jablonszky M, Szász E, Markó G, Torok J, Herczeg G, Garamszegi LZ (2017) Escape ability and risk-taking behaviour in a Hungarian population of the collared flycatcher (Ficedula Albicollis). Behav Ecol Sociobiol 71(3):54.  https://doi.org/10.1007/s00265-017-2276-6 CrossRefGoogle Scholar
  22. Kano F, Call J, Tomonaga M (2012) Face and eye scanning in gorillas (Gorilla Gorilla), orangutans (pongo abelii), and humans (Homo Sapiens): unique eye-viewing patterns in humans among hominids. J Comp Psychol 126(4):388–398.  https://doi.org/10.1037/a0029615 CrossRefPubMedGoogle Scholar
  23. Katz HK, Lustig A, Lev-Ari T, Nov Y, Rivlin E, Katzir G (2015) Eye movements in chameleons are not truly independent - evidence from simultaneous monocular tracking of two targets. J Exp Biol 218(13):2097–2105.  https://doi.org/10.1242/jeb.113084 CrossRefPubMedGoogle Scholar
  24. Kroodsma DE, Byers BE, Goodale E, Johnson S, Liu W (2001) Pseudoreplication in playback experiments, revisited a decade later. Anim Behav 61(5):1029–1033.  https://doi.org/10.1006/anbe.2000.1676 CrossRefGoogle Scholar
  25. Land MF (1999a) Motion and vision: why animals move their eyes. J Comp Physiol A 185(4):341–352.  https://doi.org/10.1007/s003590050393 CrossRefPubMedGoogle Scholar
  26. Land MF (1999b) The roles of head movements in the search and capture strategy of a tern (Aves, Laridae). J Comp Physiol A 184(3):265–272.  https://doi.org/10.1007/s003590050324 CrossRefGoogle Scholar
  27. Land MF (2015) Eye movements of vertebrates and their relation to eye form and function. J Comp Physiol A 201(2):195–214.  https://doi.org/10.1007/s00359-014-0964-5 CrossRefGoogle Scholar
  28. Larsson ML (2015) Binocular vision, the optic chiasm, and their associations with vertebrate motor behavior. Front Ecol Evol 3:89.  https://doi.org/10.3389/fevo.2015.00089 CrossRefGoogle Scholar
  29. Loretto M-C, Schloegl C, Bugnyar T (2010) Northern bald ibises follow others’ gaze into distant space but not behind barriers. Biol Lett 6(1):14–17.  https://doi.org/10.1098/rsbl.2009.0510 CrossRefPubMedGoogle Scholar
  30. Lustig A, Keter-Katz H, Katzir G (2012) Threat perception in the chameleon (Chamaeleo Chameleon): evidence for lateralized eye use. Anim Cogn 15(4):609–621.  https://doi.org/10.1007/s10071-012-0489-7 CrossRefPubMedGoogle Scholar
  31. Maldonado PE, Maturana H, Varela FJ (1988) Frontal and lateral visual system in birds. Frontal and lateral gaze. Brain. Behav Ecol 32(1):57–62.  https://doi.org/10.1159/000116532 CrossRefGoogle Scholar
  32. Martin GR (1986) The eye of a passeriform bird, the European starling (Sturnus Vulgaris): eye movement amplitude, visual fields and schematic optics. J Comp Physiol A 159(4):545–557.  https://doi.org/10.1007/BF00604174 CrossRefGoogle Scholar
  33. Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148(S2):547–562.  https://doi.org/10.1007/s10336-007-0213-6 CrossRefGoogle Scholar
  34. Martinez-Conde S, Macknik SL, Hubel DH (2004) The role of fixational eye movements in visual perception. Nat Rev Neurosci 5(3):229–240.  https://doi.org/10.1038/nrn1348 CrossRefPubMedGoogle Scholar
  35. Martinoya C, Le-Houezec J, Bloch S (1984) Pigeon’s eyes converge during feeding: evidence for frontal binocular fixation in a lateral-eyed bird. Neurosci Lett 45(3):335–339.  https://doi.org/10.1016/0304-3940(84)90248-9 CrossRefPubMedGoogle Scholar
  36. Moore BA, Pita D, Tyrrell LP, Fernández-Juricic E (2015) Vision in avian emberizid foragers: maximizing both binocular vision and fronto-lateral visual acuity. J Exp Biol 218(9):1347–1358.  https://doi.org/10.1242/jeb.108613 CrossRefPubMedGoogle Scholar
  37. Ochs MF, Zamani M, Rodrigues M, Gomes G (2017) The Auk.: Sneak peek: raptors search for prey using stochastic head turns. J Avian Med Surg 31(1):85–87Google Scholar
  38. Ohayon S, Harmening W, Wagner H, Rivlin E (2008) Through a barn owl’s eyes: interactions between scene content and visual attention. Biol Cybern 98(2):115–132.  https://doi.org/10.1007/s00422-007-0199-4 CrossRefPubMedGoogle Scholar
  39. Pyle P (1997) Identification guide to north American birds. Slate Creek Press, Point Reyes StationGoogle Scholar
  40. Qadri MA, Reid S, Cook RG (2016) Complex conditional control by pigeons in a continuous virtual environment. J Exp Anal Behav 105(1):211–229.  https://doi.org/10.1002/jeab.195 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73(2):236–253.  https://doi.org/10.1006/brln.2000.2305 CrossRefPubMedGoogle Scholar
  42. Rogers LJ, Vallortigara G, Andrew RJ (2013) Divided brains: the biology and behaviour of brain asymmetries. Cambridge University Press, CambridgeGoogle Scholar
  43. Saleh CN, Ehrlich D (1984) Composition of the supraoptic decussation of the chick (Gallus Gallus): a possible factor limiting interhemispheric transfer of visual information. Cell Tissue Res 236(3):601–609CrossRefPubMedGoogle Scholar
  44. Schmidt J, Scheid C, Kotrschal K, Bugnyar T, Schloegl C (2011) Gaze direction – a cue for hidden food in rooks (Corvus Frugilegus)? Behav Process 88(2):88–93.  https://doi.org/10.1016/j.beproc.2011.08.002 CrossRefGoogle Scholar
  45. Shaw RC, Clayton NS (2013) Careful cachers and prying pilferers: Eurasian jays (Garrulus Glandarius) limit auditory information available to competitors. Proc R Soc B 280(1752):20122238.  https://doi.org/10.1098/rspb.2012.2238 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Temple SE (2011) Why different regions of the retina have different spectral sensitivities: a review of mechanisms and functional significance of intraretinal variability in spectral sensitivity in vertebrates. Vis Neurosci 28(04):281–293.  https://doi.org/10.1017/S0952523811000113 CrossRefPubMedGoogle Scholar
  47. Templeton JJ, Christensen-Dykema JM (2008) A behavioral analysis of prey detection lateralization and unilateral transfer in European starlings (Sturnus Vulgaris). Behav Process 79(3):125–131.  https://doi.org/10.1016/j.beproc.2008.06.003 CrossRefGoogle Scholar
  48. Templeton JJ, Gonzalez DP (2004) Reverse lateralization of visual discriminative abilities in the European starling. Anim Behav 67(4):783–788.  https://doi.org/10.1016/j.anbehav.2003.04.011 CrossRefGoogle Scholar
  49. Treves A (2000) Theory and method in studies of vigilance and aggregation. Anim Behav 60(6):711–722.  https://doi.org/10.1006/anbe.2000.1528 CrossRefPubMedGoogle Scholar
  50. Tyrrell LP, Butler SR, Fernández-Juricic E (2015) Oculomotor strategy of an avian ground forager: tilted and weakly yoked eye saccades. J Exp Biol 218(16):2651–2657.  https://doi.org/10.1242/jeb.122820 CrossRefPubMedGoogle Scholar
  51. Tyrrell LP, Butler SR, Yorzinski JL, Fernández-Juricic E (2014) A novel system for bi-ocular eye-tracking in vertebrates with laterally placed eyes. Methods Ecol Evol 5(10):1070–1077.  https://doi.org/10.1111/2041-210X.12249 CrossRefGoogle Scholar
  52. Voss J, Bischof H-J (2003) Regulation of ipsilateral visual information within the tectofugal visual system in zebra finches. J Comp Physiol A 189(7):545–553.  https://doi.org/10.1007/s00359-003-0430-2 CrossRefGoogle Scholar
  53. Walls GL (1942) The vertebrate eye and it’s adaptive radiation. Cranbrook Institute of Science, Bloomfield HillsGoogle Scholar
  54. Yorzinski JL, Patricelli GL, Babcock JS, Pearson JM, Platt ML (2013) Through their eyes: selective attention in peahens during courtship. J Exp Biol 216(16):3035–3046.  https://doi.org/10.1242/jeb.087338 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Shannon R. Butler
    • 1
  • Jennifer J. Templeton
    • 2
  • Esteban Fernández-Juricic
    • 1
  1. 1.Department of Biological SciencesPurdue UniversityWest LafayetteUSA
  2. 2.Department of BiologyKnox CollegeGalesburgUSA

Personalised recommendations