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Inner-Ear Morphology of the New Zealand Kiwi (Apteryx mantelli) Suggests High-Frequency Specialization

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Abstract

The sensory systems of the New Zealand kiwi appear to be uniquely adapted to occupy a nocturnal ground-dwelling niche. In addition to well-developed tactile and olfactory systems, the auditory system shows specializations of the ear, which are maintained along the central nervous system. Here, we provide a detailed description of the auditory nerve, hair cells, and stereovillar bundle orientation of the hair cells in the North Island brown kiwi. The auditory nerve of the kiwi contained about 8,000 fibers. Using the number of hair cells and innervating nerve fibers to calculate a ratio of average innervation density showed that the afferent innervation ratio in kiwi was denser than in most other birds examined. The average diameters of cochlear afferent axons in kiwi showed the typical gradient across the tonotopic axis. The kiwi basilar papilla showed a clear differentiation of tall and short hair cells. The proportion of short hair cells was higher than in the emu and likely reflects a bias towards higher frequencies represented on the kiwi basilar papilla. The orientation of the stereovillar bundles in the kiwi basilar papilla showed a pattern similar to that in most other birds but was most similar to that of the emu. Overall, many features of the auditory nerve, hair cells, and stereovilli bundle orientation in the kiwi are typical of most birds examined. Some features of the kiwi auditory system do, however, support a high-frequency specialization, specifically the innervation density and generally small size of hair-cell somata, whereas others showed the presumed ancestral condition similar to that found in the emu.

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References

  • Bang BG, Cobb S (1968) Size of olfactory bulb in 108 species of birds. Auk 85:55–61

    Google Scholar 

  • Boord RL (1969) The anatomy of the avian auditory system. Ann NY Acad Sci 169:186–198

    Article  Google Scholar 

  • Cobb S (1960) A note on the size of the avian olfactory bulb. Epilepsia 1:394–402

    Article  PubMed  CAS  Google Scholar 

  • Corfield JR, Kubke MF, Parsons S, Wild JM, Köppl C (2011) Evidence for an auditory fovea in the New Zealand kiwi (Apteryx mantelli). PLoS One 6(8):e23771. doi:101371/journalpone00237716

    Article  PubMed  CAS  Google Scholar 

  • Counter SA, Tsao P (1986) Morphology of the seagull's inner ear. Acta Otolaryngol 101:34–42

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Davies S (2002) Ratites and tinamous.Oxford University Press Inc., New York

    Google Scholar 

  • Fischer FP (1992) Quantitative analysis of the innervation of the chicken basilar papilla. Hear Res 61:167–178

    Article  PubMed  CAS  Google Scholar 

  • Fischer FP (1994a) General pattern and morphological specializations of the avian cochlea. Scanning Microsc 8:351–363

    PubMed  CAS  Google Scholar 

  • Fischer FP (1994b) Quantitative TEM analysis of the barn owl basilar papilla. Hear Res 73:1–15

    Article  PubMed  CAS  Google Scholar 

  • Fischer FP (1998) Hair cell morphology and innervation in the basilar papilla of the emu (Dromaius novaehollandiae). Hear Res 121:112–124

    Article  PubMed  CAS  Google Scholar 

  • Fischer FP, Köppl C, Manley GA (1988) The basilar papilla of the barn owl Tyto alba: a quantitative morphological SEM analysis. Hear Res 34:87–101

    Article  PubMed  CAS  Google Scholar 

  • Fischer FP, Eisensamer B, Manley GA (1994) Cochlear and lagenar ganglia of the chicken. J Morphol 220:71–83

    Article  PubMed  CAS  Google Scholar 

  • Fuchs P, Zidanic M, Michaels R, Yuhas W, Jiang GJ (1998) Ion channels and synaptic function in chick cochlear hair cells. In: Palmer AR, Rees A, Summerfield AQ, Meddis R (eds) Psychophysical and psychological advances in hearing. Whurr Published Ltd, London, pp 97–104

    Google Scholar 

  • Gleich O, Manley GA (1988) Quantitative morphological analysis of the sensory epithelium of the starling and pigeon basilar papilla. Hear Res 34:69–85

    Article  PubMed  CAS  Google Scholar 

  • Gleich O, Manley GA (2000) The hearing organ of birds and crocodilia. In: Dooling RJ, Fay R, Popper A (eds) Comparative hearing: birds and reptiles. Springer-Verlag, New York, pp 70–138

    Google Scholar 

  • Gleich O, Manley GA, Mandl A, Dooling RJ (1994) Basilar papilla of the canary and zebra finch: a quantitative scanning electron microscopical description. J Morphol 221:1–24

    Article  Google Scholar 

  • Gleich O, Dooling RJ, Ryals BM (2001) A quantitative analysis of the nerve fibers in the VIIIth nerve of Belgian Waterslager canaries with a hereditary sensorineural hearing loss. Hear Res 151:141–148

    Article  PubMed  CAS  Google Scholar 

  • Gleich O, Fischer FP, Köppl C, Manley GA (2004) Hearing organ evolution and specialization: Archosaurs. In: Manley GA, Popper A, Fay RR (eds) Evolution of the vertebrate auditory system. Springer Verlag, New York, pp 224–255

    Chapter  Google Scholar 

  • Jorgensen JM, Christensen JT (1989) The inner ear of the common rhea (Rhea americana L.).Brain Behav Evol 34:273–280

    Article  PubMed  CAS  Google Scholar 

  • Köppl C (1997) Number and axon calibres of cochlear afferents in the barn owl. Aud Neurosci 3:313–344

    Google Scholar 

  • Köppl C (2001) Efferent axons in the avian auditory nerve. Eur J Neurosci 13:1889–1901

    Article  PubMed  Google Scholar 

  • Köppl C (2011) Evolution of the octavolateral efferent system. In: Ryugo D, Fay RR, Popper AN (eds) Auditory and vestibular efferents. Springer Science + Business Media, LLC, New York, pp 217–259

    Chapter  Google Scholar 

  • Köppl C, Manley GA (1997) Frequency representation in the emu basilar papilla. J Acoust Soc Am 101:1574–1584

    Google Scholar 

  • Köppl C, Gleich O, Manley GA (1993) An auditory fovea in the barn owl cochlea. J Comp Physiol A 171:695–704

    Article  Google Scholar 

  • Köppl C, Gleich O, Schwabedissen G, Siegl E, Manley GA (1998) Fine structure of the basilar papilla of the emu: implications for the evolution of avian hair-cell types. Hear Res 126:99–112

    Article  PubMed  Google Scholar 

  • Köppl C, Wegscheider A, Gleich O, Manley GA (2000) A quantitative study of cochlear afferent axons in birds. Hear Res 139:123–143

    Article  PubMed  Google Scholar 

  • MacLeod KM, Soares D, Carr CE (2006) Interaural timing difference circuits in the auditory brainstem of the emu (Dromaius novaehollandiae). J Comp Neurol 495:185–201

    Article  PubMed  Google Scholar 

  • Manley GA, Schwabedissen G, Gleich O (1993) Morphology of the basilar papilla of the Budgerigar, Melopsittacus undulatus. J Morphol 218:153–165

    Article  Google Scholar 

  • Manley GA, Meyer B, Fischer FP, Schwabedissen G, Gleich O (1996) Surface morphology of basilar papilla of the tufted duck Aythya fuligula, and domestic chicken Gallus gallus domesticus. J Morphol 227:197–212

    Article  PubMed  CAS  Google Scholar 

  • Martin GR, Wilson KJ, Martin Wild J, Parsons S, Fabiana Kubke M, Corfield J (2007) Kiwi forego vision in the guidance of their nocturnal activities. PLoS One 2(2):e198. doi:101371/journalpone00001982

    Article  PubMed  Google Scholar 

  • Smolders JW, Ding-Pfennigdorff D, Klinke R (1995) A functional map of the pigeon basilar papilla: correlation of the properties of single auditory nerve fibres and their peripheral origin. Hear Res 92:151–169

    Article  PubMed  CAS  Google Scholar 

  • Takasaka T, Smith CA (1971) The structure and innervation of the pigeon's basilar papilla. J Ultrastruct Res 35:20–65

    Article  PubMed  CAS  Google Scholar 

  • Tilney LG, Saunders JC (1983) Actin filaments, stereocilia, and hair cells of the bird cochlea. I. Length, number, width, and distribution of stereocilia of each hair cell are related to the position of the hair cell on the cochlea. J Cell Biol 96:807–821

    Article  PubMed  CAS  Google Scholar 

  • Tilney LG, Tilney MS (1986) Functional organization of the cytoskeleton. Hear Res 22:55–77

    Article  PubMed  CAS  Google Scholar 

  • Tilney M, Tilney L, DeRosier D (1987) The distribution of hair cell bundle lengths and orientations suggest an unexpected pattern of hair cell stimulation in the chick cochlea. Hear Res 25:141–151

    Article  PubMed  CAS  Google Scholar 

  • Wenzel BM (1968) Olfactory prowess of the kiwi. Nature 220:1133–1134

    Article  PubMed  CAS  Google Scholar 

  • Wenzel BM (1971) Olfactory sensation in the kiwi and other birds. Ann N Y Acad Sci 188:183–193

    Article  PubMed  CAS  Google Scholar 

  • Winter P (1963) Vergleichende qualitative und quantitative Untersuchungen an der Hörbahn von Vögeln. Z Morphol Ökol Tiere 52:365–400

    Article  Google Scholar 

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Acknowledgments

We wish to first thank C. Gardner and the New Zealand Department of Conservation and B. Gartrell at the Massey University College of Veterinary Medicine for their assistance in procuring specimens. We would also like to thank Hillary Holloway and the staff at the Biomedical Imaging Research Unit, the Electron and Light Microscopy Unit, and the Research Centre for Surface and Material Sciences at the University of Auckland, and the Electron Microscopy Unit at the University of Sydney for help with the Scanning Electron Microscopy.

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Authors and Affiliations

  1. Department of Anatomy with Radiology, University of Auckland, Auckland, New Zealand

    Jeremy R. Corfield & M. Fabiana Kubke

  2. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    Jeremy R. Corfield & Stuart Parsons

  3. Institute for Biology and Environmental Sciences, and Research Center Neurosensory Science, Carl von Ossietzky University, 26129, Oldenburg, Germany

    Christine Köppl

  4. Department of Neuroscience, University of Lethbridge, Lethbridge, AB, T1K3M4, Canada

    Jeremy R. Corfield

Authors
  1. Jeremy R. Corfield
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  2. M. Fabiana Kubke
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  3. Stuart Parsons
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  4. Christine Köppl
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Correspondence to Jeremy R. Corfield.

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Corfield, J.R., Kubke, M.F., Parsons, S. et al. Inner-Ear Morphology of the New Zealand Kiwi (Apteryx mantelli) Suggests High-Frequency Specialization. JARO 13, 629–639 (2012). https://doi.org/10.1007/s10162-012-0341-4

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  • DOI: https://doi.org/10.1007/s10162-012-0341-4

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