Anatomical specializations for enhanced olfactory sensitivity in Kiwi, Apteryx mantelli

Brain, Behavior and Evolution

Volumn 84, Issue 3, 2014, Pages 214-226

  Corfield, Jeremy R ^a,b,d   Eisthen, Heather L ^b   Iwaniuk, Andrew N ^c   Parsons, Stuart ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF LETHBRIDGE   (Canada)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Allometry; Brain evolution; Comparative neuroanatomy; Olfaction; Olfactory bulb; Olfactory epithelium

Indexed keywords

APTERYX AUSTRALIS MANTELLI;

ANATOMY AND HISTOLOGY; ANIMAL; BIRD; BRAIN; COMPARATIVE STUDY; CYTOLOGY; ODOR; OLFACTORY BULB;

ANIMALS; BRAIN; OLFACTORY BULB; PALAEOGNATHAE; SMELL;

EID: 84910091103     PISSN: 00068977     EISSN: 14219743     Source Type: Journal    
DOI: 10.1159/000365564     Document Type: Article

References (107)

1. Alma S, Bee De Speroni N (1992) : Indices cerebrales y composicion cuantativa encefalica en Athene cunicularia y Tyto alba. Facenas 9: 19-37.
2. Ashwell KWS, Scofield RP (2008) : Big birds and their brains: Paleoneurology of the New Zealand moa. Brain Behav Evol 71: 151-166.
3. Bang BG (1960) : Anatomical evidence for olfactory function in some species of birds. Nature 188: 547-549.
4. Bang BG (1971) : Functional anatomy of the olfactory system in 23 orders of birds. Acta Anat 79: 1-76.
5. Bang BG, Cobb S (1968) : Size of olfactory bulb in 108 species of birds. Auk 85: 55-61.
6. Barton RA, Purvis A, Harvey PH (1995) : Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Phil Trans R Soc Lond B Biol Sci 348: 381-392.
7. Benham WB (1906) : The olfactory sense in Apteryx. Nature 74: 222-223.
8. Bertelli S, Porzecanski AL (2004) : Tinamou (Tinamidae) systematics: A preliminary combined analysis of morphology and molecules. Ornitologia Neotrop 15: 1-8.
9. Blomberg SP, Garland T Jr, Ives AR (2003) : Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57: 717-745.
10. Boire D (1989) : Comparaison quantitative de l'encéphale, de ses grandes subdivisions et des relais visuels, trijemeaux et acoustiques chez 28 espèces d'oiseaux; PhD thèse, Université de Montréal, Montréal.
11. Bonadonna F, Bretagnolle V (2002) : Smelling home: A good solution for burrow-finding in nocturnal petrels? J Exp Biol 205: 2519-2523.
12. Bonadonna F, Cunningham GB, Jouventin P, Hesters F, Nevitt GA (2003b) : Evidence for nest-odour recognition in two species of diving petrel. J Exp Biol 206: 3719-3722.
13. Bonadonna F, Hesters F, Jouventin P (2003a) : Scent of a nest: Discrimination of own-nest odours in Antarctic prions, Pachyptila desolata. Behav Ecol Sociobiol 54: 174-178.
14. Bonadonna F, Miguel E, Grosbois V, Jouventin P, Bessiere JM (2007) : Individual odor recognition in birds: An endogenous olfactory signature on petrels' feathers? J Chem Ecol 33: 1819-1829.
15. Bonadonna F, Nevitt GA (2004) : Partner-specific odor recognition in an Antarctic seabird. Science 306: 835.
16. Bonadonna F, Villafane M, Bajzak C, Jouventin P (2004) : Recognition of burrow's olfactory signature in blue petrels, Halobaena caerulea: An efficient discrimination mechanism in the dark. Anim Behav 67: 893-898.
17. Burrows CJ (1989) : Moa browsing: Evidence from the Pyramid Valley mire. NZ J Ecol 12: 51-56.
18. Carezzano FJ, Bee De Speroni N (1995) : Composicion volumetrica encefalica e indices cerebrales en tres aves de ambiente acuatico (Ardeidae, Podicipedidae, Rallidae) . Facena 11: 75-83.
19. Caro SP, Balthazart J (2010) : Pheromones in birds: Myth or reality? J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196: 751-766.
20. 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.
21. Clark L, Avilova KV, Bean NJ (1993) : Odor thresholds in passerines. Comp Biochem Physiol A Comp Physiol 104: 305-312.
22. Cobb S (1960a) : A note on the size of the avian olfactory bulb. Epilepsia 1: 394-402.
23. Cobb S (1960b) : Observations on the comparative anatomy of the avian brain. Perspect Biol Med 3: 383-408.
24. Colbourne RM (1983) : A banding study of North Island brown kiwis in an exotic forest. Notornis 30: 109-124.
25. Corfield JR (2009) : Evolution of the Brain and Sensory Systems of the Kiwi; PhD thesis, University of Auckland, Auckland.
26. Corfield JR, Birkhead TR, Spottiswoode CN, Iwaniuk AN, Boogert NJ, Gutierrez-Ibanez C, Overington SE, Wylie DR, Lefebvre L (2012c) : Brain size and morphology of the brood-parasitic and cerophagous honeyguides (Aves: Piciformes) . Brain Behav Evol 81: 170-186.
27. Corfield JR, Kubke MF, Parsons S, Koppl C (2012a) : Inner-ear morphology of the New Zealand kiwi (Apteryx mantelli) suggests high-frequency specialization. J Assoc Res Otolaryngol 13: 629-639.
28. Corfield J, Kubke MF, Parsons S, Wild JM, Koppl C (2011) : Evidence for an auditory fovea in the New Zealand kiwi (Apteryx mantelli) . PLoS One 6: E23771.
29. Corfield JR, Wild JM, Hauber ME, Parsons S, Kubke MF (2008) : Evolution of brain size in the Palaeognath lineage, with an emphasis on New Zealand ratites. Brain Behav Evol 71: 87-99.
30. Corfield JR, Wild JM, Parsons S, Kubke MF (2012b) : Morphometric analysis of telencephalic structure in a variety of Neognath and Paleognath bird species reveals regional differences associated with specific behavioral traits. Brain Behav Evol 80: 181-195.
31. Craigie EH (1930) : Studies on the brain of the kiwi (Apteryx australis) . J Comp Neurol 49: 223-357.
32. 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.
33. 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.
34. 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.
35. 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.
36. Davies SJJF (2003a) : Emus; in Hutchins M (ed) : Grzimek's Animal Life Encyclopedia: 8 Birds I Tinamous and Ratites to Hoatzins. Farmington Hills, Gale Group, pp 83-87.
37. Davies SJJF (2003b) : Moas; in Hutchins M (ed) : Grzimek's Animal Life Encyclopedia: 8 Birds I Tinamous and Ratites to Hoatzins. Farmington Hills, Gale Group, pp 95-98.
38. De Leon A, Minguez E, Belliure B (2003) : Selfodour recognition in European storm-petrel chicks. Behaviour 140: 925-933.
39. Donne-Gousse C, Laudet V, Hanni C (2002) : A molecular phylogeny of anseriformes based on mitochondrial DNA analysis. Mol Phylogenet Evol 23: 339-356.
40. Ebinger P, Lohmer R (1984) : Comparative quantitative investigations on brains of rock doves, domestic and urban pigeons (Columba l. livia) . Z Zool Syst Evol 22: 136-145.
41. Ebinger P, Lohmer R (1987) : A volumetric comparison of brains between greylag geese ( Anser anser L.) and domestic geese. J Hirnforsch 28: 291-299.
42. Ericson PGP, Jansén A, Johansson US, Ekman J (2005) : Inter-generic relationships of the crows, jays, magpies and allied groups (Aves: Corvidae) based on nucleotide sequence data. J Avian Biol 36: 222-234.
43. Fernandez P, Carezzano F, Bee De Speroni N (1997) : Análisis cuantitativo encefálico e índices cerebrales en Aratinga acuticaudata y Myiopsitta monachus de Argentina (Aves: Psittacidae) . Rev Chil Hist Nat 70: 269-275.
44. Firestein S (2001) : How the olfactory system makes sense of scents. Nature 413: 211-218.
45. Frelinger AL 3rd, Rutishauser U (1986) : Topography of N-CAM structural and functional determinants. 2. Placement of monoclonal antibody epitopes. J Cell Biol 103: 1729-1737.
46. Garland T, Ives AR (2000) : Using the past to predict the present: Confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155: 346-364.
47. Gittleman JL (1991) : Carnivore olfactory bulb size: Allometry, phylogeny and ecology. J Zool 225: 253-272.
48. Graves GR (1992) : The greater yellow-headed vulture (Cathartes melambrotus) locates food by olfaction. J Raptor Res 26: 38-39.
49. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) : A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763-1768.
50. Hagelin JC (2004) : Observations on the olfactory ability of the Kakapo Strigops habroptilus, the critically endangered parrot of N. Z. Ibis 146: 161-164.
51. Hagelin JC, Jones IL, Rasmussen LEL (2003) : A tangerine-scented social odour in a monogamous seabird. Proc Biol Sci 270: 1323-1329.
52. Harriman AE, Berger RH (1986) : Olfactory acuity in the common raven (Corvus corax) . Physiol Behav 36: 257-262.
53. Harvey PH, Pagel MD (1991) : The comparative method in evolutionary biology. Oxford, Oxford University Press.
54. Healy S, Guilford T (1990) : Olfactory bulb size and nocturnality in birds. Evolution 44: 339-346.
55. Hill A (1905) : Can birds smell? Nature 71: 318-319.
56. Holland RA, Thorup K, Gagliardo A, Bisson IA, Knecht E, Mizrahi D, Wikelski M (2009) : Testing the role of sensory systems in the migratory heading of a songbird. J Exp Biol 212: 4065-4071.
57. Hutchison LV, Wenzel BM (1980) : Olfactory guidance in foraging by procellariiforms. Condor 82: 314-319.
58. Iwaniuk AN, Dean KM, Nelson JE (2004) : A mosaic pattern characterizes the evolution of the avian brain. Proc Biol Sci 271: 148-151.
59. Kavoi BM, Jameela H (2011) : Comparative morphometry of the olfactory bulb, tract and stria in the human, dog and goat. Int J Morphol 29: 939-946.
60. Kraabe KH (1959) : Studies on the brain development of the kiwi Apteryx mantelli. Copenhagen, Munksgaard.
61. Lavin SR, Karasov WH, Ives AR, Middleton KM, Garland T Jr (2008) : Morphometrics of the avian small intestine compared with that of nonflying mammals: A phylogenetic approach. Physiol Biochem Zool 81: 526-550.
62. Maddison WP, Maddison DR (2011) : Mesquite: A modular system for evolutionary analysis -version 275. http: //mesquiteprojectorg. Martin GR, Wilson KJ, Martin Wild J, Parsons S
63. Fabiana Kubke M, Corfield J (2007) : Kiwi forego vision in the guidance of their nocturnal activities. PLoS One 2: E198.
64. Mayr G (2011) : The phylogeny of charadriiform birds (shorebirds and allies) -reassessing the conflict between morphology and molecules. Zool J Linn Soc 161: 916-934.
65. Mehlhorn J, Hunt GR, Gray RD, Rehkamper G, Gunturkun O (2010) : Tool-making New Caledonian crows have large associative brain areas. Brain Behav Evol 75: 63-70.
66. Michelsen WJ (1959) : Procedure for studying olfactory discrimination in the pigeon. Science 130: 630-631.
67. Midford PE, Garland TJ, Maddison W (2010) : PDAP: PDTREE package for Mesquite. v1.15. http: //mesquiteprojec.org/pdap-mesquite/.
68. Nevitt GA (1999) : Olfactory foraging in Antarctic seabirds: A species-specific attraction to krill odors. Mar Ecol Prog Ser 177: 235-241.
69. Nevitt GA, Reid K, Trathan P (2004) : Testing olfactory strategies in an Antarctic seabird assemblage. J Exp Biol 207: 3537-3544.
70. Nevitt GA, Veit RR, Kareiva P (1995) : Dimethyl sulfide as a foraging clue for Antarctic procellariiform seabirds. Nature 376: 680-682.
71. Nieuwenhuys R (1967) : Comparative anatomy of the olfactory centers and tracts; in Zotterman Y (ed) : Progress in Brain Research. Amsterdam, Elsevier, pp 1-64.
72. Owen R (1839) : On the anatomy of the Southern Apteryx ( Apteryx australis, Shaw) . J Zool 2: 257-301.
73. Papi F (1990) : Olfactory navigation in birds. Experientia 46: 352-363.
74. Parker TJ (1891) : Observations on the anatomy and development of Apteryx. Phil Trans R Soc Lond B Biol Sci 182: 25-134.
75. Pistone E, Carezzano F, Bee De Speroni N (2002) : Tamaño relativo encefálico e índices cerebrales en Vanellus c. chilensis (Aves: Charadriidae) . Rev Chil Hist Nat 75: 595-602.
76. Portmann A (1947) : Etudes sur la cérébralisation chez les oiseaux. 2. Les indices intra cérébraux. Alauda 15: 1-15.
77. Potter MA (1989) : Ecology and Reproductive Biology of the North Island Brown Kiwi (Apteryx australis mantelli) ; PhD thesis, Massey University, Palmerston North.
78. Rehkamper G, Frahm HD, Zilles K (1991) : Quantitative development of brain and brain structures in birds (Galliformes and Passeriformes) compared to that in mammals (insectivores and primates) . Brain Behav Evol 37: 125-143.
79. 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. NZ J Ecol 5: 76-85.
80. Revell LJ (2009) : Size-correction and principal components for interspecific comparative studies. Evolution 63: 3258-3268.
81. Roper TJ (1999) : Olfaction in birds. Adv Study Behav 28: 247-332.
82. Roper TJ (2003) : Olfactory discrimination in yellow-backed chattering lories Lorius garrulus flavopalliatus: First demonstration of olfaction in Psittaciformes. Ibis 145: 689-691.
83. Smith SA, Paselk RA (1986) : Olfactory sensitivity of the turkey vulture (Cathartes aura) to three carrion associated odorants. Auk 103: 586-592.
84. Snyder GK, Peterson TT (1979) Olfactory sensitivity in the black-billed magpie and in the pigeon. Comp Biochem Physiol 62: 921-925.
85. Soini HA, Whittaker DJ, Wiesler D, Ketterson ED, Novotny MV (2013) : Chemosignaling diversity in songbirds: Chromatographic profiling of preen oil volatiles in different species. J Chromatogr A 1317: 186-192.
86. Stattleman AJ, Talbot RB, Coulter DB (1975) : Olfactory thresholds of pigeon (Columba livia) , quail (Colinus virginianus) and chickens (Gallus gallus) . Comp Biochem Physiol 50A: 807-809.
87. Steiger SS, Fidler AE, Kempenaers B (2009) : Evidence for increased olfactory receptor gene repertoire size in two nocturnal bird species with well-developed olfactory ability. BMC Evol Biol 9: 117.
88. Steiger SS, Fidler AE, Valcu M, Kempenaers B (2008) : Avian olfactory receptor gene repertoires: Evidence for a well-developed sense of smell in birds? Proc Biol Sci 275: 2309-2317.
89. Taborsky B, Taborsky M (1995) : Habitat use and selectivity by the brown kiwi (Apteryx australis mantelli) in a patchy environment. Auk 112: 680-689.
90. Team RC (2013) : R: A language and environment for statistical computing. http: //www. r-project.org/.
91. Tucker D (1965) : Electrophysiological evidence for olfactory function in birds. Nature 207: 34-36.
92. Waldvogel JA (1989) : Olfactory orientation by birds. Curr Ornithol 1: 269-321.
93. Walker JC, Walker DB, Tambiah CR, Gilmore KS (1986) : Olfactory and non-olfactory odor detection in pigeons: Elucidation by a cardiac acceleration paradigm. Physiol Behav 38: 575-580.
94. Wallraff HG (2003) : Olfactory navigation by birds. J Ornithol 144: 1-32.
95. Wallraff HG (2004) : Avian olfactory navigation: Its empirical foundation and conceptual state. Anim Behav 67: 189-204.
96. Wang N, Kimball RT, Braun EL, Liang B, Zhang Z (2013) : Assessing phylogenetic relationships among Galliformes: A multigene phylogeny with expanded taxon sampling in Phasianidae. PLoS One 8: E64312.
97. Watanabe M, Frelinger AL 3rd, Rutishauser U (1986) : Topography of N-CAM structural and functional determinants. 1. Classification of monoclonal antibody epitopes. J Cell Biol 103: 1721-1727.
98. Watt JC (1971) : The North Island kiwi: A predator of pasture insects. NZ Entomol 5: 25-27.
99. Wenzel BM (1968) : Olfactory prowess of the kiwi. Nature 220: 1133-1134.
100. Wenzel BM (1971) : Olfactory sensation in the kiwi and other birds. Ann NY Acad Sci 188: 183-193.
101. Wenzel BM (1987) : The olfactory and related systems in birds. Ann NY Acad Sci 519: 137-149.
102. Wenzel BM, Meisami E (1987) : Number, size, and density of mitral cells in the olfactory bulbs of the Northern Fulmar and Rock Dove. Ann NY Acad Sci 510: 700-702.
103. Whittaker DJ, Gerlach NM, Soini HA, Novotny MV, Ketterson ED (2013) : Bird odour predicts reproductive success. Anim Behav 86: 697-703.
104. Whittaker DJ, Richmond KM, Miller AK, Kiley R, Burns CB, Atwell JW, Ketterson ED (2011) : Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis) . Behav Ecol 22: 1256-1263.
105. Wright TF, Schirtzinger EE, Matsumoto T, Eberhard JR, Graves GR, Sanchez JJ, Capelli S, Muller H, Scharpegge J, Chambers GK, Fleischer RC (2008) : A multilocus molecular phylogeny of the parrots (Psittaciformes) : Support for a Gondwanan origin during the cretaceous. Mol Biol Evol 25: 2141-2156.
106. Yopak KE, Lisney TJ, Collin SP (2014) : Not all sharks are 'swimming noses': Variation in olfactory bulb size in cartilaginous fishes. Brain Struct Funct DOI: 10.1007/s00429-014-0705-0.
107. Zelenitsky DK, Therrien F, Ridgely RC, McGee AR, Witmer LM (2011) : Evolution of olfaction in non-avian theropod dinosaurs and birds. Proc Biol Sci 278: 3625-3634.