Journal of Comparative Physiology A

, Volume 199, Issue 4, pp 263–277 | Cite as

Interspecific differences in the visual system and scanning behavior of three forest passerines that form heterospecific flocks

  • Bret A. Moore
  • Megan Doppler
  • Jordan E. Young
  • Esteban Fernández-Juricic
Original Paper


Little is known as to how visual systems and visual behaviors vary within guilds in which species share the same micro-habitat types but use different foraging tactics. We studied different dimensions of the visual system and scanning behavior of Carolina chickadees, tufted titmice, and white-breasted nuthatches, which are tree foragers that form heterospecific flocks during the winter. All species had centro-temporally located foveae that project into the frontal part of the lateral visual field. Visual acuity was the highest in nuthatches, intermediate in titmice, and the lowest in chickadees. Chickadees and titmice had relatively wide binocular fields with a high degree of eye movement right above their short bills probably to converge their eyes while searching for food. Nuthatches had narrower binocular fields with a high degree of eye movement below their bills probably to orient the fovea toward the trunk while searching for food. Chickadees and titmice had higher scanning (e.g., head movement) rates than nuthatches probably due to their wider blind areas that limit visual coverage. The visual systems of these three species seem tuned to the visual challenges posed by the different foraging and scanning strategies that facilitate the partitioning of resources within this guild.


Foraging Fovea Vigilance Visual acuity Visual fields 


  1. Bartmess-LeVasseur J, Branch CL, Browning SA, Owens JL, Freeberg TM (2010) Predator stimuli and calling behavior of Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis). Behav Ecol Sociobiol 64:1187–1198CrossRefGoogle Scholar
  2. Beauchamp G (2003) Group-size effects on vigilance: a search for mechanisms. Behav Process 63:111–121CrossRefGoogle Scholar
  3. Blackwell BF, Fernández-Juricic E, Seamans TW, Dolan T (2009) Avian visual system configuration and behavioural response to object approach. Anim Behav 77:673–684CrossRefGoogle Scholar
  4. Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer Associates Inc, SunderlandGoogle Scholar
  5. Carr JM, Lima SL (2012) Heat-conserving postures hinder escape: a thermoregulation—predation trade-off in wintering birds. Behav Ecol 23:434–441CrossRefGoogle Scholar
  6. Changizi MA, Shimojo S (2008) ‘‘X-ray vision’’ and the evolution of forward-facing eyes. J Theor Biol 254:756–767PubMedCrossRefGoogle Scholar
  7. Collin SP (1999) Behavioural ecology and retinal cell topography. In: Archer S, Djamgoz MB, Loew E, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Kluwer Academic Publishers, Dordrecht, pp 509–535Google Scholar
  8. Dolan T, Fernández-Juricic E (2010) Retinal ganglion cell topography of five species of ground foraging birds. Brain Behav Evol 75:111–121PubMedCrossRefGoogle Scholar
  9. Dolby AS, Grubb TC Jr (1998) Benefits to satellite members in mixed species foraging groups: an experimental analysis. Anim Behav 56:501–509PubMedCrossRefGoogle Scholar
  10. Dolby AS, Grubb TC Jr (2000) Social context affects risk taking by satellite species in a mixed-species foraging group. Behav Ecol 11:110–114CrossRefGoogle Scholar
  11. Dunlap K, Mowrer OH (1930) Head movements and eye functions of birds. J Comp Psychol 11:99–112CrossRefGoogle Scholar
  12. Dunning JB Jr (2008) CRC handbook of avian body masses, 2nd edn. CRC Press, Taylor and Francis Group, LondonGoogle Scholar
  13. Ehrlich D (1981) Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. J Comp Neurol 195:643–657PubMedCrossRefGoogle Scholar
  14. Fernández-Juricic E (2012) Sensory basis of vigilance behavior in birds: synthesis and future prospects. Behav Process 89:143–152CrossRefGoogle Scholar
  15. Fernández-Juricic E, Blumstein DT, Abrica G, Manriquez L, Adams LB, Adams R, Daneshrad M, Rodriguez-Prieto I (2006) Relationships of anti-predator escape and post-escape responses with body mass and morphology: a comparative avian study. Evol Ecol Res 8:731–752Google Scholar
  16. Fernández-Juricic E, Gall MD, Dolan T, Tisdale V, Martin GR (2008) The visual fields of two ground-foraging birds, house finches and house sparrows, allow for simultaneous foraging and anti-predator vigilance. Ibis 150:779–787CrossRefGoogle Scholar
  17. Fernández-Juricic E, O’Rourke C, Pitlik T (2010) Visual coverage and scanning behavior in two corvid species: American crow and Western scrub jay. J Comp Physiol A 196:879–888CrossRefGoogle Scholar
  18. Fernández-Juricic E, Gall MD, Dolan T, O’Rourke C, Thomas S, Lynch JR (2011a) Visual systems and vigilance behaviour of two ground-foraging avian prey species: white-crowned sparrows and California towhees. Anim Behav 81:705–713CrossRefGoogle Scholar
  19. Fernández-Juricic E, Moore BA, Doppler M, Freeman J, Blackwell BF, Lima SL, DeVault TL (2011b) Testing the terrain hypothesis: Canada geese see their world laterally and obliquely. Brain Behav Evol 77:147–158PubMedCrossRefGoogle Scholar
  20. Fernández-Juricic E, Beauchamp G, Treminio R, Hoover M (2011c) Making heads turn: association between head movements during vigilance and perceived predation risk in brown-headed cowbird flocks. Anim Behav 82:573–577CrossRefGoogle Scholar
  21. Fite KV, Rosenfield-Wessels S (1975) A comparative study of deep avian foveas. Brain Behav Evol 12:97–115PubMedCrossRefGoogle Scholar
  22. Freeman B, Tancred E (1978) The number and distribution of ganglion cells in the retina of the brush-tailed possum, Trichosurus vulpecula. J Comp Neurol 177:557–567PubMedCrossRefGoogle Scholar
  23. Frens K (2010) Effects of food type and patch location on foraging in local birds: a field test of optimal foraging predictions. Masters thesis, University of Michigan.
  24. Friedman MB (1975) How birds use their eyes. In: Wright P, Caryl P, Vowles DM (eds) Neural and endocrine aspects of behavior in birds. Elsevier, Amsterdam, pp 182–204Google Scholar
  25. Gall MD, Fernández-Juricic E (2009) Effects of physical and visual access to prey on patch selection and food search effort in a sit-and-wait predator, the Black Phoebe. Condor 111:150–158CrossRefGoogle Scholar
  26. Garamszegi LZ, Møller AP, Erritzøe J (2002) Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc R Soc Lond B 269:961–967CrossRefGoogle Scholar
  27. Gioanni H (1988) Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic eye (OKN) and head (OCR) reflexes. Exp Brain Res 69:567–582PubMedCrossRefGoogle Scholar
  28. Grubb TC Jr, Pravasudov VV (1994) Tufted Titmouse (Baeolophus bicolor). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. doi:10.2173/bna.86 Google Scholar
  29. Grubb TC Jr, Pravasudov VV (2008) White-breasted Nuthatch (Sitta carolinensis). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. doi:10.2173/bna.54 Google Scholar
  30. Guillemain M, Martin GR, Fritz H (2002) Feeding methods, visual fields and vigilance in dabbling ducks (Anatidae). Func Ecol 16:522–529CrossRefGoogle Scholar
  31. Hart NS (2001) Variations in cone photoreceptor abundance and the visual ecology of birds. J Comp Physiol A 187:685–698PubMedCrossRefGoogle Scholar
  32. Heesy CP (2004) On the relationship between orbit orientation and binocular visual field overlap in mammals. Anat Rec 281A:1104–1110CrossRefGoogle Scholar
  33. Heesy CP (2009) Seeing in stereo: the ecology and evolution of primate binocular vision and stereopsis. Evol Anthropol 18:21–35CrossRefGoogle Scholar
  34. Henry KS, Lucas JR (2008) Coevolution of auditory sensitivity and temporal resolution with acoustic signal space in three songbirds. Anim Behav 76:1659–1671CrossRefGoogle Scholar
  35. Howland HC, Merola S, Basarab JR (2004) The allometry and scaling of the size of vertebrate eyes. Vision Res 44:2043–2065PubMedCrossRefGoogle Scholar
  36. Hughes A (1977) The topography of vision in mammals of contrasting life style: comparative optics and retinal organization. In: Crescitelli F (ed) The visual system in vertebrates. Springer-Verlag, New York, pp 615–756Google Scholar
  37. Iwaniuk AN, Heesy CP, Hall MI, Wylie DR (2008) Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds. J Comp Physiol A 194:267–282CrossRefGoogle Scholar
  38. Kiltie RA (2000) Scaling of visual acuity with body size in mammals and birds. Func Ecol 14:226–234CrossRefGoogle Scholar
  39. Lima SL (1992) Vigilance and foraging substrate: anti-predatory considerations in a non-standard environment. Behav Ecol Sociobiol 30:283–289CrossRefGoogle Scholar
  40. Lima SL (1993) Ecological and evolutionary perspectives on escape from predatory attack: a survey of North American birds. Wilson Bull 105:1–47Google Scholar
  41. Martin GR (1984) The visual fields of the tawny owl, Strix aluco L. Vision Res 24:1739–1751PubMedCrossRefGoogle Scholar
  42. Martin GR (1993) Producing the image. In: Zeigler HP, Bischof H-J (eds) Vision, brain and behaviour in birds. MIT press, Massachusetts, pp 5–24Google Scholar
  43. Martin GR (1998) Eye structure and amphibious foraging in albatrosses. Proc Royal Soc B 265:665–671CrossRefGoogle Scholar
  44. Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148:S547–S562CrossRefGoogle Scholar
  45. Martin GR (2009) What is binocular vision for? A birds’ eye view. J Vision 9:1–19CrossRefGoogle Scholar
  46. Martin GR, Coetzee HC (2004) Visual fields in hornbills: precision-grasping and sunshades. Ibis 146:18–26CrossRefGoogle Scholar
  47. Martin GR, Prince PA (2001) Visual fields and foraging in Procellariiform seabirds: sensory aspects of dietary segregation. Brain Behav Evol 57:33–38PubMedCrossRefGoogle Scholar
  48. Martin GR, Rojas LM, Figueroa YMR, McNeil R (2004) Binocular vision and nocturnal activity in oilbirds (Steatornis caripensis) and Pauraques (Nyctidromus albicollis) Caprimulgiformes. Ornitol Neotrop 15(Suppl):233–242Google Scholar
  49. Martin GR, Jarrett N, Williams M (2007) Visual fields in blue ducks Hymenolaimus malacorhynchos and pink-eared ducks Malacorhynchus membranaceus: visual and tactil foraging. Ibis 149:112–120CrossRefGoogle Scholar
  50. McIlwain JT (1996) An introduction to the biology of vision. Cambridge University Press, New YorkCrossRefGoogle Scholar
  51. Meyer DBC (1977) The avian eye and its adaptations. In: Crescitelli F (ed) The visual system of vertebrates, handbook of sensory physiology. Springer, New York, pp 549–612CrossRefGoogle Scholar
  52. Møller AP, Erritzøe J (2010) Flight distance and eye size in birds. Ethol 116:458–465CrossRefGoogle Scholar
  53. Moroney MK, Pettigrew JD (1987) Some observations on the visual optics of kingfishers (Aves, Coraciformes, Alcedinidae). J Comp Physiol A 160:137–149CrossRefGoogle Scholar
  54. Mostrom AM, Curry RL, Lohr B (2002) Carolina chickadee (Poecile carolinensis). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. doi:10.2173/bna.636 Google Scholar
  55. O’Rourke CT, Hall MI, Pitlik T, Fernández-Juricic E (2010a) Hawk eyes I: diurnal raptors differ in visual fields and degree of eye movement. PLoS ONE 5:e12802PubMedCrossRefGoogle Scholar
  56. O’Rourke CT, Pitlik T, Hoover M, Fernández-Juricic E (2010b) Hawk eyes II: diurnal raptors differ in head movement strategies when scanning from perches. PLoS ONE 5:e12169PubMedCrossRefGoogle Scholar
  57. Pettigrew JD, Dreher B, Hopkins CS, Mccall MJ, Brown M (1988) Peak density and distribution of ganglion-cells in the retinae of Microchiropteran bats—implications for visual-acuity. Brain Behav Evol 32:39–56PubMedCrossRefGoogle Scholar
  58. Reymond L (1985) Spatial visual acuity of the eagle, Aquila audax: a behavioural, optical and anatomical investigation. Vision Res 25:1477–1491PubMedCrossRefGoogle Scholar
  59. Schwab IR (2012) How eyes evolved. Evolution’s witness. Oxford University Press, OxfordGoogle Scholar
  60. Siemers BM, Swift SM (2006) Differences in sensory ecology contribute to resource partitioning in the bats Myotis bechsteinii and Myotis nattereri (Chiroptera: Vespertilionidae). Behav Ecol Sociobiol 59:373–380CrossRefGoogle Scholar
  61. Simberloff D, Dayan T (1991) The guild concept and the structure of ecological communities. Annu Rev Ecol Evol Syst 22:115–143CrossRefGoogle Scholar
  62. Stone J (1981) The wholemount handbook. A guide to the preparation and analysis of retinal wholemounts. Maitland Publishing, SydneyGoogle Scholar
  63. Sullivan KA (1984a) Information exploitation by downy woodpeckers in mixed-species flocks. Behav 91:294–311CrossRefGoogle Scholar
  64. Sullivan KA (1984b) The advantages of social foraging in downy woodpeckers. Anim Behav 32:16–22CrossRefGoogle Scholar
  65. Templeton CN, Greene E (2007) Nuthatches eavesdrop on variations in heterospecific chickadee mobbing alarm calls. Proc Natl Academy Sci USA 104:5479–5482CrossRefGoogle Scholar
  66. Troscianko J, von Bayern AM, Chappell J, Rutz C, Martin GR (2012) Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows. Nat Commun 3:1110PubMedCrossRefGoogle Scholar
  67. Ullmann JFP, Moore BA, Temple SE, Fernández-Juricic E, Collin SP (2012) The retinal wholemount technique: a window to understanding the brain and behaviour. Brain Behav Evol 79:26–44PubMedCrossRefGoogle Scholar
  68. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, MichiganCrossRefGoogle Scholar
  69. Wathey JC, Pettigrew JD (1989) Quantitative analysis of the retinal ganglion cell layer and optic nerve of the Barn Owl Tyto alba. Brain Behav Evol 33:279–292PubMedCrossRefGoogle Scholar
  70. Williams DR, Coletta NJ (1987) Cone spacing and the visual resolution limit. J Opt Soc Am A 4:1514–1523PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Bret A. Moore
    • 1
  • Megan Doppler
    • 1
  • Jordan E. Young
    • 1
  • Esteban Fernández-Juricic
    • 1
  1. 1.Department of Biological SciencesPurdue UniversityWest LafayetteUSA

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