Birds with larger eyes are predicted to have higher spatial resolution because of their larger retinal image. Raptors are well known for their acute vision, mediated by their deep central fovea. Because foraging strategies may demand specific visual adaptations, eye size and fovea may differ between species with different foraging ecology. We tested whether predators (actively hunting mobile prey) and carrion eaters (eating dead prey) from the order Accipitriformes differ in eye size, foveal depth, and retinal thickness using spectral domain optical coherence tomography and comparative phylogenetic methods. We found that (1) all studied predators (except one) had a central and a temporal fovea, but all carrion eaters had only the central fovea; (2) eye size scaled with body mass both in predators and carrion eaters; (3) predators had larger eyes relative to body mass and a thicker retina at the edge of the fovea than carrion eaters, but there was no difference in the depth of the central fovea between the groups. Finally, we found that (4) larger eyes generally had a deeper central fovea. These results suggest that the visual system of raptors within the order Accipitriformes may be highly adapted to the foraging strategy, except for the foveal depth, which seems mostly dependent upon the eye size.

1.
Aslam TM, Haider D, Murray IJ (2007): Principles of disability glare measurement: an ophthalmological perspective. Acta Ophthalmol Scand 85:354-360.
2.
Bang BG, Cobb S (1968): The size of the olfactory bulb in 108 species of birds. Auk 85:55-61.
3.
Brooke MdL, Hanley S, Laughlin S (1999): The scaling of eye size with body mass in birds. Proc R Soc Lond B 266:405-412.
4.
Buckley NJ (1996): Food finding and the influence of information, local enhancement, and communal roosting on foraging success of North American vultures. Auk 113:473-488.
5.
Burton RF (2008): The scaling of eye size in adult birds: relationship to brain, head and body sizes. Vision Res 48:2345-2351.
6.
Buttery RG, Colin FL, Hinrichsen W, Weller L, Haight JR (1991): How thick should a retina be? A comparative study of mammalian species with and without intraretinal vasculature. Vision Res 31:169-187.
7.
Chen Y, Lan W, Schaeffel F (2015): Size of the foveal blue scotoma related to the shape of the foveal pit but not to macular pigment. Vision Res 106:81-89.
8.
Coimbra JP, Collin SP, Hart NS (2015): Variations in retinal photoreceptor topography and the organization of the rod-free zone reflect behavioral diversity in Australian passerines. J Comp Neurol 523:1073-1094.
9.
Del Hoyo J, Sargatal J, Elliot A (eds) (1994): Handbook of the Birds of the World. Barcelona, Lynx Edicions, Vol 2: New World Vultures to Guineafowl.
10.
Deygout C, Gault A, Duriez O, Sarrazin F, Bessa-Gomes C (2010): Impact of food predictability on social facilitation by foraging scavengers. Behav Ecol 21:1131-1139.
11.
Drea CM, Vignieri SN, Cunningham SB, Glickman SE (2002): Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): I. Investigation of environmental odors and the function of rolling. J Comp Psychol 116:331-341.
12.
Dunning JB (2007): CRC Handbook of Avian Body Mass, ed 2. Boca Raton, CRC Press.
13.
Fischer AB (1969): Laboruntersuchungen und Freilandbeobachtungen zum Sehvermögen und Verhalten von Altweltgeiern. Zool Jahrb Sys 96:81-132.
14.
Fite KV, Rosenfield-Wessels S (1975): A comparative study of deep avian foveas. Brain Behav Evol 12:97-115.
15.
Freckleton RP, Harvey PH, Pagel M (2002): Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712-726.
16.
Gilbert M, Chansocheat S (2006): Olfaction in accipitrid vultures. Vulture News 55:6-7.
17.
Gomez LG, Houston DC, Cotton P, Tye A (1994): The role of greater yellow-headed vultures Cathartes melambrotus as scavengers in neotropical forest. Ibis 136:193-196.
18.
Hall MI, Ross CF (2007): Eye shape and activity pattern in birds. J Zool 271:437-444.
19.
Harmening WM, Vobig MA, Walter P, Wagner H (2007): Ocular aberrations in barn owl eyes. Vision Res 47:2934-2942.
20.
Hendrickson AE, Yuodelis C (1984): The morphological development of the human fovea. Ophthalmology 91:603-612.
21.
Hirsch J (1982): Falcon visual sensitivity to grating contrast. Nature 300:57-58.
22.
Houston DC (1974): Food searching in griffon vultures. Afr J Ecol 12:63-77.
23.
Houston DC (1986): Scavenging efficiency of turkey vultures in tropical forest. Condor 88:318-323.
24.
Howland HC, Merola S, Basarab JR (2004): The allometry and scaling of the size of vertebrate eyes. Vision Res 44:2043-2065.
25.
Hughes A (1977): The topography of vision in mammals of contrasting life style: comparative optics and retinal organisation; in Crescitelli F (ed): Handbook of Sensory Physiology. Berlin, Springer, vol. VII/5, pp 613-756.
26.
Inzunza O, Bravo H, Smith RL, Angel M (1991): Topography and morphology of retinal ganglion cells in falconiforms: a study on predatory and carrion-eating birds. Anat Rec 229:271-277.
27.
Jackson AL, Ruxton GD, Houston DC (2008): The effect of social facilitation on foraging success in vultures: a modelling study. Biol Lett 4:311-313.
28.
Jeffery G, Williams A (1994): Is abnormal retinal development in albinism only a mammalian problem? Normality of a hypopigmented avian retina. Exp Brain Res 100:47-57.
29.
Jiang L, Chen J, Wang P, Ren Q, Yuan J, Qian C, Hua X, Guo Z, Zhang L, Yang J (2015): The mitochondrial genomes of Aquila fasciata and Buteo lagopus (Aves, Accipitriformes): sequence, structure and phylogenetic analyses. PLoS One 10:e0136297.
30.
Jonas JB, Ohno-Matsui K, Holbach L, Panda-Jonas S (2017): Association between axial length and horizontal and vertical globe diameters. Graefes Arch Clin Exp Ophthalmol 255:237-242.
31.
Jones MP, Pierce KE, Ward D (2007): Avian vision: a review of form and function with special consideration to birds of prey. J Exotic Pet Med 16:69-87.
32.
Kiltie R (2000): Scaling of visual acuity with body size in mammals and birds. Funct Ecol 14:226-234.
33.
Koch DD (1989): Glare and contrast sensitivity testing in cataract patients. J Cataract Refract Surg 15:158-164.
34.
Land MF, Nilsson DE (2012): Animal Eyes. Oxford, Oxford University Press.
35.
Lisney TJ, Stecyk K, Kolominsky J, Graves GR, Wylie DR, Iwaniuk AN (2013): Comparison of eye morphology and retinal topography in two species of New World vultures (Aves: Cathartidae). Anat Rec 296:1954-1970.
36.
Locket NA (1992): Problems of deep foveas. Aust NZ J Ophthalmol 20:281-295.
37.
Maier FM, Howland HC, Ohlendorf A, Wahl S, Schaeffel F (2015): Lack of oblique astigmatism in the chicken eye. Vision Res 109:68-76.
38.
Martin GR (2007): Visual fields and their functions in birds. J Ornithol 148:547-562.
39.
Martin GR (2014): The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds. Philos Trans R Soc B Biol Sci 369:20130040.
40.
Martin GR, Katzir G (2000): Sun shades and eye size in birds. Brain Behav Evol 56:340-344.
41.
McIsaac HP (2001): Raptor acuity and wind turbine blade conspicuity. Proceedings of the National Avian-Wind Power Planning Meeting IV. Washington, Resolve, pp 59-87.
42.
Mitkus M, Chaib S, Lind O, Kelber A (2014): Retinal ganglion cell topography and spatial resolution of two parrot species: budgerigar (Melopsittacus undulatus) and Bourke's parrot (Neopsephotus bourkii). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 200:371-384.
43.
Mitkus M, Nevitt GA, Danielsen J, Kelber A (2016): Vision on the high seas: spatial resolution and optical sensitivity in two procellariiform seabirds with different foraging strategies. J Exp Biol 219:3329-3338.
44.
Mitkus M, Olsson P, Toomey MB, Corbo JC, Kelber A (2017): Specialized photoreceptor composition in the raptor fovea. J Comp Neurol 525:2152-2163.
45.
Moran D, Softley R, Warrant E (2015): The energetic cost of vision and the evolution of eyeless Mexican cavefish. Sci Adv 1:e1500363.
46.
Niven JE, Laughlin SB (2008): Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 2008;211(11):1792-1804.
47.
Oehme H (1964): Vergleichende Untersuchungen an Greifvogelaugen. Z Morph Ökol Tiere 53:618-635.
48.
Orme D (2013): The caper package: comparative analysis of phylogenetics and evolution in R. R package version 5. https://cran.r-project.org/web/packages/caper/index.html.
49.
Ott M, Schaeffel F (1995): A negatively powered lens in the cameleon. Nature 373:692-694.
50.
Paradis E, Strimmer K, Claude J, Jobb G, Opgen-Rhein R, Dutheil J, Noel Y, Bolker B, Lemon J (2008): The ape package. Analyses of phylogenetics and evolution. https://cran.r-project.org/web/packages/ape/index.html.
51.
Pinheiro J, Bates D, DebRoy S, Sarkar D (2014): R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117. http://CRAN.R-project.org/package=nlme.
52.
Potier S, Bonadonna F, Kelber A, Duriez O (2016a): Visual acuity in an opportunistic raptor, the chimango caracara (Milvago chimango). Physiol Behav 157:125-128.
53.
Potier S, Bonadonna F, Kelber A, Martin GR, Isard PF, Dulaurent T, Duriez O (2016b): Visual abilities in two raptors with different ecology. J Exp Biol 291:2639-2649.
54.
Pumphrey R (1948): The theory of the fovea. J Exp Biol 25:299-312.
55.
Querubin A, Lee HR, Provis JM, O'Brien KMB (2009): Photoreceptor and ganglion cell topographies correlate with information convergence and high acuity regions in the adult pigeon (Columba livia) retina. J Comp Neurol 517:711-722.
56.
R Development Core Team (2015) The R Project for Statistical Computing. http://www.cran.r-project.org/.
57.
Rasband WS (1997-2012) Image J. Bethesda, US National Institutes of Health, http://imagej.nih.gov/ij/.
58.
Reymond L (1985): Spatial visual acuity of the eagle Aquila audax: a behavioural, optical and anatomical investigation. Vision Res 25:1477-1491.
59.
Reymond L (1987): Spatial visual acuity of the falcon, Falco berigora: a behavioural, optical and anatomical investigation. Vision Res 27:1859-1874.
60.
Ritland SM (1982): The Allometry of the Vertebrate Eye; PhD thesis, University of Chicago.
61.
Rochon-Duvigneaud A (1919): Quelques données sur la fovea des oiseaux. Ann Oculist (Paris) 46:1-16.
62.
Rochon-Duvigneaud A (1943): Les yeux et la vision des vertébrés. Paris, Masson.
63.
Ruggeri M, Major JC Jr, McKeown C, Knighton RW, Puliafito CA, Jiao S (2010): Retinal structure of birds of prey revealed by ultra-high resolution spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 51:5789-5795.
64.
Shlaer R (1972): An eagle's eye: quality of the retinal image. Science 176:920-922.
65.
Smith SA, Paselk RA (1986): Olfactory sensitivity of the turkey vulture (Cathartes aura) to three carrion-associated odorants. Auk 103:586-592.
66.
Snyder AW, Miller WH (1978): Telephoto lens system of falconiform eyes. Nature 275:127-129.
67.
Tucker VA (2000): The deep fovea, sideways vision and spiral flight paths in raptors. J Exp Biol 203:3745-3754.
68.
Valentin G (1879): Ein Beitrag zur Kenntnis der Brechungsverhältnisse der Tiergewebe. Pflügers Arch Ges Physiol 19:78-105.
69.
Walls GL (1937): Significance of the foveal depression. Arch Ophthalmol 18:912.
70.
Walls GL (1942): The Vertebrate Eye and Its Adaptive Radiation. Blooming Hills, Cranbrook Institute.
71.
Wells MC, Lehner PN (1978): The relative importance of the distance senses in coyote predatory behaviour. Anim Behav 26:251-258.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.