Retinal Anatomy of the New Zealand Kiwi: Structural Traits Consistent With Their Nocturnal Behavior

Anatomical Record

Volumn 298, Issue 4, 2015, Pages 771-779

  Corfield, Jeremy R ^a   Parsons, Stuart ^a   Harimoto, Yoshitetsu ^b   Acosta, Monica L ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Barn Owl; Kiwi; Nocturnal; Photoreceptors; Retina

Indexed keywords

ADULT; ANATOMICAL VARIATION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINOCULAR VISION; BIRD; BRAIN REGION; CONTROLLED STUDY; DIURNAL SPECIES; EYE; EYE SIZE; KIWI; LIGHT; LIGHT ADAPTATION; NOCTURNAL SPECIES; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR INNER SEGMENT; PRIORITY JOURNAL; RETINA; RETINA ROD; RETINAL THICKNESS; TISSUE SECTION; VISION; VISUAL SYSTEM; ANATOMY AND HISTOLOGY; ANIMAL; EVOLUTION; NEW ZEALAND; ODOR; PHYSIOLOGY; RATITE; VISUAL FIELD;

APTERYX; AVES; TYTONIDAE;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; NEW ZEALAND; PALAEOGNATHAE; RETINA; SMELL; VISUAL FIELDS; VISUAL PERCEPTION;

EID: 84925379529     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.23080     Document Type: Article

References (66)

1. Acosta ML, Kalloniatis M, Christie DL. 2005. Creatine transporter localization in developing and adult retina: importance of creatine to retinal function. Am J Physiol Cell Physiol 289:1015-1023.
2. Bang BG, Cobb S. 1968. Size of olfactory bulb in 108 species of birds. Auk 85:55-61.
3. Blough DS. 1955. Method for tracing dark adaptation in the pigeon. Science 121:703-704.
4. Bowmaker JK, Martin GR. 1978. Visual pigments and colour vision in a nocturnal bird, Strix aluco (tawny owl). Vision Res 18:1125-1130.
5. Bridges CDB, Quilliam TA. 1973. Visual pigments of men, moles and hedgehogs. Vision Res 13:2417-2421.
6. Buckley K, Kelly RB. 1985. Identification of a transmembrane glycoprotein specific for secretory vesicles of neuronal and endocrine cells. J Cell Biol 100:1284-1294.
7. Buller WL. 1888. A history of the birds of New Zealand. London: Taylor and Francis.
8. Castro I, Cunningham SJ, Gsell AC, Jaffe K, Cabrera A, Liendo C. 2010. Olfaction in birds: a closer look at the kiwi (Apterygidae). J Avian Biol 41:213-218.
9. Colbourne RM, Kleinpaste R. 1984. North Island brown kiwi vocalisations and their use in censuring populations. Notornis 31:191-201.
10. Corfield J, Gillman L, Parsons S. 2008. Vocalizations of the North Island brown kiwi (Apteryx mantelli). Auk 125:326-335.
11. Corfield J, Kubke MF, Parsons S, Wild JM, Koppl C. 2011a. Evidence for an auditory fovea in the New Zealand kiwi (Apteryx mantelli). PLoS ONE 6:e23771.
12. Corfield JR, Eisthen HL, Iwaniuk AN, Parsons S. 2014. Anatomical specialisations for enhanced olfactory sensitivity in kiwi, Apteryx mantelli. Brain Behav Evol. DOI: 10.1159/000365564.
13. Corfield JR, Gsell AC, Brunton D, Heesy CP, Hall MI, Acosta ML, Iwaniuk AN. 2011b. Anatomical specializations for nocturnality in a critically endangered parrot, the Kakapo (Strigops habroptilus). PLoS One 6:e22945.
14. Corfield JR, Kubke MF, Parsons S, Koppl C. 2012. Inner-ear morphology of the New Zealand kiwi (Apteryx mantelli) suggests high-frequency specialization. J Assoc Res Otolaryngol 13:629-639.
15. Craigie EH. 1930. Studies on the brain of the kiwi (Apteryx australis). J Comp Neurol 49:223-357.
16. Cserháti P, Szél A, Röhlich P. 1989. Four cone types characterized by anti-visual pigment antibodies in the pigeon retina. Invest Ophthalmol Vis Sci 30:74-81.
17. Cunningham SJ, Alley MR, Castro I. 2010. Facial bristle feather histology and morphology in New Zealand birds: implications for function. J Morphol 272:118-128.
18. Cunningham SJ, Castro I, Alley M. 2007. A new prey-detection mechanism for kiwi (Apteryx spp.) suggests convergent evolution between paleognathous and neognathous birds. J Anat 211:493-502.
19. Cunningham SJ, Castro I, Potter MA. 2009. The relative importance of olfaction and remote touch in prey detection by North Island brown kiwis. Anim Behav 78:899-905.
20. Cunningham SJ, Corfield JR, Iwaniuk AN, Castro I, Alley MR, Birkhead TR, Parsons S. 2013. The anatomy of the bill tip of kiwi and associated somatosensory regions of the brain: comparisons with shorebirds. PLoS ONE 8:e80036.
21. Fischer AJ, Dierks BD, Reh TA. 2002. Exogenous growth factors induce the production of ganglion cells at the retinal margin. Development 129:2283-2291.
22. Fosser NS, Brusco A, Rios H. 2005. Darkness induced neuroplastic changes in the serotoninergic system of the chick retina. Brain Res Dev Brain Res 160:211-218.
23. 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 269:961-967.
24. Glösmann M, Steiner M, Peichl L, Peter A. 2008. Cone photoreceptors and potential UV vision in a subterranean insectivore, the European mole. J Vis 8:1-12.
25. Hall MI, Ross CF. 2006. Eye shape and activity pattern in birds. J Zool 271:437-444.
26. Hart NS. 2001. The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675-703.
27. Hetling JR, Baig-Silva MS, Comer CM, Pardue MT, Samaan DY, Qtaishat NM, Pepperberg DR, Park TJ. 2005. Features of visual function in the naked mole-rat Heterocephalus glaber. J Comp Physiol A 191:317-330.
28. Horvat-Brocker A, Reinhard J, Illes S, Paech T, Zoidl G, Harroch S, Distler C, Knyazev P, Ullrich A, Faissner A. 2008. Receptor protein tyrosine phosphatases are expressed by cycling retinal progenitor cells and involved in neuronal development of mouse retina. Neuroscience 152:618-645.
29. Husband S, Shimizu T. 2001. Evolution of the avian visual system. In: Cook RG, editor. Avian visual cognition. Medford, MA: Tufts University.
30. Johannesson-Gross K. 1988. Brightness discrimination of the mole (Talpa europaea L.) in learning experiments applying a modified tube-maze method. Z Saugetierk 53:193-201.
31. Kojima D, Okano T, Fukada Y, Shichida Y, Yoshizawa T, Ebrey TG. 1992. Cone visual pigments are present in gecko rod cells. Proc Natl Acad Sci U S A 89:6841-6845.
32. Kronfeld-Schor N, Dayan T, Jones ME, Kremer I, Mandelik Y, Wollberg M, Yassur Y, Gaton DD. 2001. Retinal structure and foraging microhabitat use of the golden spiny mouse (Acomys russatus). J Mammal 82:1016-1025.
33. Land MF, Nilsson DE. 2002. Animal eyes. Oxford: Oxford University Press.
34. Lima IP, Saito K, Hamassaki DE, Yan CY. 2007. Immunohistochemical characterization of the chick marginal retina. Braz J Med Biol Res 40:1455-1464.
35. Lund RD, Lund JS. 1965. The visual system of the mole, Talpa europaea. Exp Neurol 13:302-316.
36. Lund RD, Lund JS. 1966. The central visual pathways and their functional significance in the mole. J Zool 149:95-101.
37. Martin GR. 1986. Sensory capacities and the nocturnal habit of owls (Strigiformes). Ibis 128:266-277.
38. Martin GR. 1990. Birds by night. London: T & AD Poyser.
39. Martin GR. 1993. Producing the image. In: Zeigler HP, Bischof HJ, editors. Vision brain, and behaviour in birds. Cambridge, MA: MIT Press. p 5-24.
40. Martin GR, Gordon IE. 1974. Visual acuity in the tawny owl (Strix aluco). Vision Res 14:1393-1397.
41. Martin GR, Rojas LM, Ramirez Figueroa YM, McNeil R. 2004. Binocular vision and nocturnal activity in Oilbirds (Steatornis caripensis) and Pauraques (Nyctidromus albicollis): Caprimulgiformes. Ornithol Neotrop 15(Suppl):233-242.
42. Martin GR, Wilson KJ, Wild JM, Parsons S, Kubke MF, Corfield JR. 2007. Kiwi forego vision in the guidance of their nocturnal activities. PLoS ONE 2:e198.
43. McNeil R, McSween A, Lachapelle P. 2005. Comparison of the retinal structure and function in four bird species as a function of the time they start singing in the morning. Brain Behav Evol 65:202-214.
44. Montiani-Ferreira F, Fischer A, Cernuda-Cernuda R, Kiupel M, DeGrip WJ, Sherry D, Cho SS, Shaw GC, Evans MG, Hocking PM, Petersen-Jones SM. 2005. Detailed histopathologic characterization of the retinopathy, globe enlarged (rge) chick phenotype. Mol Vis 11:11-27.
45. Němec P, Cveková P, Benada O, Wielkopolska E, Olkowicz S, Turlejski K, Burda H, Bennett NC, Peichl L. 2008. The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex. Brain Res Bull 75:356-364.
46. Němec P, Cveková P, Burda H, Benada O, Peichl L. 2007. Visual systems and the role of vision in subterranean rodents: diversity of retinal properties and visual system designs. In: Begall S, Burda H, Schleich CE, editors. Subterranean rodents: news from underground. Heidelberg: Springer. p 129-160.
47. Orlowski J, Harmening W, Wagner H. 2012. Night vision in barn owls: visual acuity and contrast sensitivity under dark adaptation. J Vis 12:4.
48. Quilliam TA. 1964. Special features of the eye of the mole. J Anat 98:685-686.
49. Quilliam TA. 1966. The problem of vision in the ecology of Talpa europaea. Exp Eye Res 5:63-78.
50. Reid B, Ordish RG, Harrison M. 1982. An analysis of the gizzard contents of 50 north island brown kiwi (Apteryx australis mantelli) and notes on feeding observations. N Z J Ecol 5:76-85.
51. Rojas LM, McNeil R, Cabana T, Lachapelle P. 1997. Diurnal and nocturnal visual function in two tactile foraging waterbirds: the American white ibis and the black skimmer. Condor 99:191-200.
52. Rojas LM, McNeil R, Cabana T, Lachapelle P. 1999a. Behavioral, morphological and physiological correlates of diurnal and nocturnal vision in selected wading bird species. Brain Behav Evol 53:227-242.
53. Rojas LM, McNeil R, Cabana T, Lachapelle P. 1999b. Diurnal and nocturnal visual capabilities in shorebirds as a function of their feeding strategies. Brain Behav Evol 53:29-43.
54. Rojas LM, Ramírez Y, McNeil R, Mitchell M, Marín G. 2004. Retinal morphology and electrophysiology of two caprimulgiformes birds: the cave-living and nocturnal oilbird (Steatornis caripensis), and the crepuscularly and nocturnally foraging common pauraque (Nyctidromus albicollis). Brain Behav Evol 64:19-33.
55. Szél A, Takács L, Monostori E, Vigh-Teichmann I, Röhlich P. 1985. Heterogeneity of chicken photoreceptors as defined by hybridoma supernatants. An immunocytochemical study. Cell Tissue Res 240:735-741.
56. Taniguchi Y, Hisatomi O, Yoshida M, Tokunaga F. 1999. Evolution of visual pigments in geckos. FEBS Lett 445:36-40.
57. Tansley K. 1961. The retina of a diurnal gecko. Arch Gen Physiol 272:262-269.
58. Tansley K, Erichsen JR. 1985. Vision. In: Campbell B, Lack E, editors. Dictionary of birds. Calton UK: Poyser. p 623-629.
59. Thomas RJ, Szekely T, Cuthill IC, Harper DG, Newson SE, Frayling TD, Wallis PD. 2002. Eye size in birds and the timing of song at dawn. Proc Biol Sci 269:831-837.
60. Underwood G. 1951. Reptilian retinas. Nature 167:183-185.
61. Waldvogel JA. 1990. The bird's eye view. Am Sci 78:342-353.
62. Walls GL. 1934. The reptilian retina. I. A new concept of visual-cell evolution. Am J Ophthalmol 17:892-915.
63. Walls GL. 1943. The vertebrate eye and its adaptive radiation. Bloomfield Hills, Michigan: The Cranbrook Press.
64. Watt JC. 1971. The North Island kiwi: a predator of pasture insects. N Z Entomol 5:25-27.
65. Wenzel BM. 1968. Olfactory prowess of the kiwi. Nature 220:1133-1134.
66. Wilhelm M, Zhu B, Gabriel R, Straznicky C. 1993. Immunocytochemical identification of serotonin-synthesizing neurons in the vertebrate retina: a comparative study. Exp Eye Res 56:231-240.