Auditory performance in bald eagles and red-tailed hawks: a comparative study of hearing in diurnal raptors

Abstract

Collision with wind turbines is a conservation concern for eagles with population abundance implications. The development of acoustic alerting technologies to deter eagles from entering hazardous air spaces is a potentially significant mitigation strategy to diminish associated morbidity and mortality risks. As a prelude to the engineering of deterrence technologies, auditory function was assessed in bald eagles (Haliaeetus leucocephalus), as well as in red-tailed hawks (Buteo jamaicensis). Auditory brainstem responses (ABRs) to a comprehensive battery of clicks and tone bursts varying in level and frequency were acquired to evaluate response thresholds, as well as suprathreshold response characteristics of wave I of the ABR, which represents the compound potential of the VIII cranial nerve. Sensitivity curves exhibited an asymmetric convex shape similar to those of other avian species, response latencies decreased exponentially with increasing stimulus level and response amplitudes grew with level in an orderly manner. Both species were responsive to a frequency band at least four octaves wide, with a most sensitive frequency of 2 kHz, and a high-frequency limit of approximately 5.7 kHz in bald eagles and 8 kHz in red-tailed hawks. Findings reported here provide a framework within which acoustic alerting signals might be developed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Notes

  1. 1.

    The number of diurnal raptor orders is in a state of flux as both the North American Classification Committee (NACC) and the South American Classification Committee (SACC) of the American Ornithological Society have categorized New World Vultures (Cathartidae) in a separate order, the Cathartiformes, whereas the International Ornithologists’ Union currently classifies Cathartidae as a family within Accipitriformes (Chesser et al. 2019; Remsen et al. 2019; Gill and Donsker 2019). Also, Cariamiformes (seriemas), a basal order within Australaves, have been classified as diurnal raptors (Jarvis et al. 2014), although they are predominantly flightless predators.

  2. 2.

    The International Ornithologists’ Union recognizes Tyto alba pratincola as Tyto furcata pratincola (Gill and Donsker 2019).

Abbreviations

ABR:

Auditory brainstem response

AWEA:

American Wind Energy Association

ANOVA:

Analysis of variance

CAP:

Compound action potential of the auditory nerve

CN:

Cochlear nuclei

dB SPL:

Decibels sound pressure level referenced to 20 µPa

EtCO2 :

End-tidal CO2

Hz:

Hertz (cycles/s)

IPI:

Interpeak interval

IUCN:

International Union for Conservation of Nature

kHz:

KiloHertz

nMLD:

Dorsolateral mesencephalic nucleus

USDOE:

Unites States Department of Energy

USFWS:

United States Fish and Wildlife Service

USGAO:

United States Government Accountability Office

References

  1. American Wind Energy Association (AWEA) (2018) U.S. wind industry fourth quarter 2018 market report. http://www.awea.org/2018marketreports. Accessed 04 Mar 2019

  2. Barker FK, Cibois A, Schikler P et al (2004) Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci USA 101:11040–11045. https://doi.org/10.1073/pnas.0401892101

    CAS  Article  PubMed  Google Scholar 

  3. Barton L, Bailey ED, Gatehouse RW (1984) Audibility curve of bobwhite quail (Colinus virginianus). J Aud Res 24:87–97

    CAS  PubMed  Google Scholar 

  4. Beatini JR, Proudfoot GA, Gall MD (2018) Frequency sensitivity in Northern saw-whet owls (Aegolius acadicus). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 204:145–154. https://doi.org/10.1007/s00359-017-1216-2

    CAS  Article  PubMed  Google Scholar 

  5. Beston JA, Diffendorfer JE, Loss S (2015) Insufficient sampling to identify species affected by turbine collisions. J Wildl Manag 79:513–517. https://doi.org/10.1002/jwmg.852

    Article  Google Scholar 

  6. Beurg M, Tan X, Fettiplace R (2013) A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species. Neuron 79:69–81. https://doi.org/10.1016/j.neuron.2013.05.018

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 112:999–1008

    PubMed  Article  Google Scholar 

  8. Brittan-Powell EF, Lohr B, Hahn DC, Dooling RJ (2005) Auditory brainstem responses in the Eastern Screech Owl: an estimate of auditory thresholds. J Acoust Soc Am 118:314–321

    PubMed  Article  Google Scholar 

  9. Brittan-Powell EF, Dooling RJ, Ryals B, Gleich O (2010) Electrophysiological and morphological development of the inner ear in Belgian Waterslager canaries. Hear Res 269:56–69. https://doi.org/10.1016/j.heares.2010.07.003

    Article  PubMed  PubMed Central  Google Scholar 

  10. Burkard R (1991) Effects of noiseburst rise time and level on the gerbil brainstem auditory evoked response. Audiology 30:47–58

    CAS  PubMed  Article  Google Scholar 

  11. Calford MB (1988) Constraints on the coding of sound frequency imposed by the avian interaural canal. J Comp Physiol A 162:491–502

    Article  Google Scholar 

  12. Caras ML, Brenowitz E, Rubel EW (2010) Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:581–599. https://doi.org/10.1007/s00359-010-0545-1

    Article  PubMed  PubMed Central  Google Scholar 

  13. Carrete M, Sánchez-Zapata JA, Benítez JR et al (2009) Large scale risk-assessment of wind-farms on population viability of a globally endangered long-lived raptor. Biol Conserv 142:2954–2961. https://doi.org/10.1016/j.biocon.2009.07.027

    Article  Google Scholar 

  14. Chaplin SB, Diesel DA, Kasparie JA (1984) Body temperature regulation in Red-tailed hawks and Great Horned owls: responses to air temperature and food deprivation. Condor 86:175–181. https://doi.org/10.2307/1367036

    Article  Google Scholar 

  15. Chen L, Salvi R, Shero M (1994) Cochlear frequency-place map in adult chickens: intracellular biocytin labeling. Hear Res 81:130–136

    CAS  PubMed  Article  Google Scholar 

  16. Chesser RT, Burns KJ, Cicero C et al (2019) Check-list of North American Birds (online). American Ornithological Society. http://checklist.aou.org/taxa. Accessed 04 Mar 2019

  17. Church MW, Shucard DW (1987) Pentobarbital-induced changes in the mouse brainstem auditory evoked potential as a function of click repetition rate and time postdrug. Brain Res 403:72–81. https://doi.org/10.1016/0006-8993(87)90124-7

    CAS  Article  PubMed  Google Scholar 

  18. Coles RB, Guppy A (1988) Directional hearing in the barn owl (Tyto alba). J Comp Physiol A 163:117–133. https://doi.org/10.1007/BF00612002

    CAS  Article  PubMed  Google Scholar 

  19. Counter SA (1985) Brain-stem evoked potentials and noise effects in seagulls. Comp Biochem Physiol A Comp Physiol 81:837–845

    CAS  PubMed  Article  Google Scholar 

  20. Crowell SE, Wells-Berlin AM, Carr CE et al (2015) A comparison of auditory brainstem responses across diving bird species. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 201:803–815. https://doi.org/10.1007/s00359-015-1024-5

    Article  PubMed  PubMed Central  Google Scholar 

  21. Crowell SE, Wells-Berlin AM, Therrien RE et al (2016) In-air hearing of a diving duck: a comparison of psychoacoustic and auditory brainstem response thresholds. J Acoust Soc Am 139:3001–3008. https://doi.org/10.1121/1.4948574

    Article  PubMed  PubMed Central  Google Scholar 

  22. de Lucas M, Ferrer M, Bechard MJ, Muñoz AR (2012) Griffon vulture mortality at wind farms in southern Spain: distribution of fatalities and active mitigation measures. Biol Conserv 147:184–189. https://doi.org/10.1016/j.biocon.2011.12.029

    Article  Google Scholar 

  23. Dmitrieva LP, Gottlieb G (1992) Development of brainstem auditory pathway in mallard duck embryos and hatchlings. J Comp Physiol A 171:665–671

    CAS  PubMed  Article  Google Scholar 

  24. Don M, Ponton CW, Eggermont JJ, Masuda A (1993) Gender differences in cochlear response time: an explanation for gender amplitude differences in the unmasked auditory brain-stem response. J Acoust Soc Am 94:2135–2148. https://doi.org/10.1121/1.407485

    CAS  Article  PubMed  Google Scholar 

  25. Dooling RJ (1979) Temporal summation of pure tones in birds. J Acoust Soc Am 65:1058–1060. https://doi.org/10.1121/1.382576

    CAS  Article  PubMed  Google Scholar 

  26. Dooling RJ, Searcy MH (1985) Temporal integration of acoustic signals by the budgerigar (Melopsittacus undulatus). J Acoust Soc Am 77:1917–1920. https://doi.org/10.1121/1.391835

    CAS  Article  PubMed  Google Scholar 

  27. Dooling RJ, Zoloth SR, Baylis JR (1978) Auditory sensitivity, equal loudness, temporal resolving power, and vocalizations in the house finch (Carpodacus mexicanus). J Comp Physiol Psychol 92:867–876

    CAS  PubMed  Article  Google Scholar 

  28. Dyson ML, Klump GM, Gauger B (1998) Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls. J Comp Physiol A 182:695–702. https://doi.org/10.1007/s003590050214

    Article  Google Scholar 

  29. Erickson WP, Johnson GD, Young DPJ (2005) A summary and comparison of bird mortality from anthropogenic causes with an emphasis on collisions. In: Ralph CJ, Rich TD (eds) 2005 Bird conservation implementation and integration in the Americas: proceedings of the third international partners in flight conference 2002 March 20–24, Asilomar, vol 2 Gen Tech Rep PSW-GTR-191. US Dept of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, pp 1029–1042

  30. Ericson PGP, Anderson CL, Britton T et al (2006) Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2:543–547. https://doi.org/10.1098/rsbl.2006.0523

    Article  PubMed  PubMed Central  Google Scholar 

  31. Fernandez KA, Jeffers PWC, Lall K et al (2015) Aging after noise exposure: acceleration of cochlear synaptopathy in “recovered” ears. J Neurosci 35:7509–7520. https://doi.org/10.1523/JNEUROSCI.5138-14.2015

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  33. 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

    CAS  PubMed  Article  Google Scholar 

  34. Gall MD, Brierley LE, Lucas JR (2011) Species and sex effects on auditory processing in brown-headed cowbirds and red-winged blackbirds. Anim Behav 81:973–982. https://doi.org/10.1016/j.anbehav.2011.01.032

    Article  Google Scholar 

  35. Garcelon DK, Martell MS, Redig PT, Buøen LC (1985) Morphometric, karyotypic, and laparoscopic techniques for determining sex in Bald Eagles. J Wildl Manag 49:595–599. https://doi.org/10.2307/3801678

    Article  Google Scholar 

  36. Garvin JC, Jennelle CS, Drake D, Grodsky SM (2011) Response of raptors to a windfarm. J Appl Ecol 48:199–209

    Article  Google Scholar 

  37. Gill F, Donsker D (eds) (2019) IOC World Bird List (v9.1). https://doi.org/10.14344/ioc.ml.9.1

  38. Gleich O (1989) Auditory primary afferents in the starling: correlation of function and morphology. Hear Res 37:255–267

    CAS  PubMed  Article  Google Scholar 

  39. Gleich O (1994) Excitation patterns in the starling cochlea: a population study of primary auditory afferents. J Acoust Soc Am 95:401–409. https://doi.org/10.1121/1.408333

    CAS  Article  PubMed  Google Scholar 

  40. Gleich O, Langemann U (2011) Auditory capabilities of birds in relation to the structural diversity of the basilar papilla. Hear Res 273:80–88. https://doi.org/10.1016/j.heares.2010.01.009

    CAS  Article  PubMed  Google Scholar 

  41. Gleich O, Dooling RJ, Manley GA (2005) Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs. Naturwissenschaften 92:595–598. https://doi.org/10.1007/s00114-005-0050-5

    CAS  Article  PubMed  Google Scholar 

  42. Goldstein MH, Kiang NY-S (1958) Synchrony of neural activity in electric responses evoked by transient acoustic stimuli. J Acoust Soc Am 30:107–114. https://doi.org/10.1121/1.1909497

    Article  Google Scholar 

  43. Grandori F (1986) Field analysis of auditory evoked brainstem potentials. Hear Res 21:51–58

    CAS  PubMed  Article  Google Scholar 

  44. Grier JW (1982) Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 218:1232–1235

    CAS  PubMed  Article  Google Scholar 

  45. Gummer AW, Smolders JW, Klinke R (1987) Basilar membrane motion in the pigeon measured with the Mössbauer technique. Hear Res 29:63–92

    CAS  PubMed  Article  Google Scholar 

  46. Hackett SJ, Kimball RT, Reddy S et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768. https://doi.org/10.1126/science.1157704

    CAS  Article  PubMed  Google Scholar 

  47. Haig SM, D’Elia J, Eagles-Smith C et al (2014) The persistent problem of lead poisoning in birds from ammunition and fishing tackle. Condor 116:408–428

    Article  Google Scholar 

  48. Hardy RW, Kinney SE, Lueders H, Lesser RP (1982) Preservation of cochlear nerve function with the aid of brain stem auditory evoked potentials. Neurosurgery 11:16–19. https://doi.org/10.1227/00006123-198207010-00004

    Article  PubMed  Google Scholar 

  49. He DZZ, Beisel KW, Chen L et al (2003) Chick hair cells do not exhibit voltage-dependent somatic motility. J Physiol (Lond) 546:511–520

    CAS  Article  Google Scholar 

  50. Hecox K, Squires N, Galambos R (1976) Brainstem auditory evoked responses in man. I. Effect of stimulus rise-fall time and duration. J Acoust Soc Am 60:1187–1192. https://doi.org/10.1121/1.381194

    CAS  Article  PubMed  Google Scholar 

  51. Henry KR (1995) Auditory nerve neurophonic recorded from the round window of the Mongolian gerbil. Hear Res 90:176–184

    CAS  PubMed  Article  Google Scholar 

  52. Henry KS, Lucas JR (2008) Coevolution of auditory sensitivity and temporal resolution with acoustic signal space in three songbirds. Anim Behav 76:1659–1671. https://doi.org/10.1016/j.anbehav.2008.08.003

    Article  Google Scholar 

  53. Henry KS, Lucas JR (2010) Auditory sensitivity and the frequency selectivity of auditory filters in the Carolina chickadee, Poecile carolinensis. Anim Behav 80:497–507. https://doi.org/10.1016/j.anbehav.2010.06.012

    Article  Google Scholar 

  54. Hunt WG, McClure CJW, Allison TD (2015) Do raptors react to ultraviolet light? J Rapt Res 49:342–343. https://doi.org/10.3356/JRR-14-71.1

    Article  Google Scholar 

  55. IUCN (2019) The IUCN Red List of Threatened Species. Version 2019-1. http://www.iucnredlist.org. Accessed 21 Mar 2019

  56. Jarvis ED, Mirarab S, Aberer AJ et al (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–1331. https://doi.org/10.1126/science.1253451

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Jewett DL, Romano MN (1972) Neonatal development of auditory system potentials averaged from the scalp of rat and cat. Brain Res 36:101–115. https://doi.org/10.1016/0006-8993(72)90769-x

    CAS  Article  PubMed  Google Scholar 

  58. Jewett DL, Williston JS (1971) Auditory-evoked far fields averaged from the scalp of humans. Brain 94:681–696. https://doi.org/10.1093/brain/94.4.681

    CAS  Article  PubMed  Google Scholar 

  59. Jewett DL, Romano MN, Williston JS (1970) Human auditory evoked potentials: possible brain stem components detected on the scalp. Science 167:1517–1518

    CAS  PubMed  Article  Google Scholar 

  60. Jones TA, Beck MM, Brown-Borg HM, Burger RE (1987) Far-field recordings of short latency auditory responses in the White Leghorn chick. Hear Res 27:67–74

    CAS  PubMed  Article  Google Scholar 

  61. Kimball RT, Wang N, Heimer-McGinn V et al (2013) Identifying localized biases in large datasets: a case study using the avian tree of life. Mol Phylogenet Evol 69:1021–1032. https://doi.org/10.1016/j.ympev.2013.05.029

    Article  PubMed  Google Scholar 

  62. Klump GM, Maier EH (1990) Temporal summation in the European starling (Sturnus vulgaris). J Comp Psychol 104:94–100. https://doi.org/10.1037/0735-7036.104.1.94

    Article  Google Scholar 

  63. Klump GM, Kretzschmar E, Curio E (1986) The hearing of an avian predator and its avian prey. Behav Ecol Sociobiol 18:317–323

    Article  Google Scholar 

  64. Knudsen EI, Konishi M (1979) Mechanisms of sound localization in the barn owl (Tyto alba). J Comp Physiol A 133:13–21. https://doi.org/10.1007/BF00663106

    Article  Google Scholar 

  65. Konishi M (1973) How the owl tracks its prey: experiments with trained barn owls reveal how their acute sense of hearing enables them to catch prey in the dark. Am Sci 61:414–424

    Google Scholar 

  66. Köppl C (1997) Number and axon calibres of cochlear afferents in the barn owl. Aud Neurosci 3:313–334

    Google Scholar 

  67. Köppl C, Gleich O (2007) Evoked cochlear potentials in the barn owl. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:601–612. https://doi.org/10.1007/s00359-007-0215-0

    Article  PubMed  Google Scholar 

  68. Köppl C, Manley GA (1997) Frequency representation in the emu basilar papilla. J Acoust Soc Am 101:1574–1584. https://doi.org/10.1121/1.418145

    Article  Google Scholar 

  69. Köppl C, Gleich O, Manley GA (1993) An auditory fovea in the barn owl cochlea. J Comp Physiol A 171:695–704. https://doi.org/10.1007/BF00213066

    Article  Google Scholar 

  70. Kraemer A, Baxter C, Hendrix A, Carr CE (2017) Development of auditory sensitivity in the barn owl. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 203:843–853. https://doi.org/10.1007/s00359-017-1197-1

    Article  PubMed  PubMed Central  Google Scholar 

  71. Krüger O, Radford AN (2008) Doomed to die? Predicting extinction risk in the true hawks Accipitridae. Anim Conserv 11:83–91. https://doi.org/10.1111/j.1469-1795.2007.00155.x

    Article  Google Scholar 

  72. Krumm B, Klump G, Köppl C, Langemann U (2017) Barn owls have ageless ears. Proc Biol Sci B 284:20171584. https://doi.org/10.1098/rspb.2017.1584

    Article  Google Scholar 

  73. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085. https://doi.org/10.1523/JNEUROSCI.2845-09.2009

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  74. Kuvlesky WP Jr, Brennan LA, Morrison ML et al (2007) Wind energy development and wildlife conservation: challenges and opportunities. J Wildl Manag 71:2487–2498

    Article  Google Scholar 

  75. Langemann U, Hamann I, Friebe A (1999) A behavioral test of presbycusis in the bird auditory system. Hear Res 137:68–76

    CAS  PubMed  Article  Google Scholar 

  76. Lehman RN, Kennedy PL, Savidge JA (2007) The state of the art in raptor electrocution research: a global review. Biol Conserv 136:159–174. https://doi.org/10.1016/j.biocon.2006.09.015

    Article  Google Scholar 

  77. Lohr B, Brittan-Powell EF, Dooling RJ (2013) Auditory brainstem responses and auditory thresholds in woodpeckers. J Acoust Soc Am 133:337–342. https://doi.org/10.1121/1.4770255

    Article  PubMed  PubMed Central  Google Scholar 

  78. Lopez-Poveda EA, Barrios P (2013) Perception of stochastically undersampled sound waveforms: a model of auditory deafferentation. Front Neurosci 7:124. https://doi.org/10.3389/fnins.2013.00124

    Article  PubMed  PubMed Central  Google Scholar 

  79. Loss SR, Will T, Marra PP (2014) Refining estimates of bird collision and electrocution mortality at power lines in the United States. PLoS One 9:e101565. https://doi.org/10.1371/journal.pone.0101565

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  80. Madders M, Whitfield DP (2006) Upland raptors and the assessment of wind farm impacts. Ibis 148:43–56

    Article  Google Scholar 

  81. Manley GA, Köppl C (1998) Phylogenetic development of the cochlea and its innervation. Curr Opin Neurobiol 8:468–474

    CAS  PubMed  Article  Google Scholar 

  82. Manley GA, Brix J, Kaiser A (1987) Developmental stability of the tonotopic organization of the chick’s basilar papilla. Science 237:655–656

    CAS  PubMed  Article  Google Scholar 

  83. Manley GA, Meyer B, Fischer FP et al (1996) Surface morphology of basilar papilla of the tufted duck Aythya fuligula, and domestic chicken Gallus gallus domesticus. J Morphol 227:197–212. https://doi.org/10.1002/(SICI)1097-4687(199602)227:2%3c197:AID-JMOR6%3e3.0.CO;2-6

    CAS  Article  PubMed  Google Scholar 

  84. Maxwell A, Hansen KA, Larsen ON et al (2016) Testing auditory sensitivity in the great cormorant (Phalacrocorax carbo sinensis): psychophysics vs. auditory brainstem response. Proc Mtgs Acoust 27:050001. https://doi.org/10.1121/2.0000261

    Article  Google Scholar 

  85. May RF, Lund PA, Langston R et al (2010) Collision risk in white-tailed eagles. Modelling collision risk using vantage point observations in Smøla wind-power plant. Norwegian Institute for Nature Research (NINA) Report 639

  86. Mayr E (1946) The number of species of birds. Auk 63:64–69

    Article  Google Scholar 

  87. Mindell DP, Fuchs J, Johnson JA (2018) Phylogeny, taxonomy, and geographic diversity of diurnal raptors: Falconiformes, Accipitriformes, and Cathartiformes. In: Sarasola JH, Grande JM, Negro JJ (eds) Birds of prey: biology and conservation in the XXI century. Springer International Publishing, Cham, pp 3–32

    Google Scholar 

  88. Mlíkovský J (1989) Brain size in birds: 2. Falconiformes through Gaviiformes. Vést cs Spolec Zool 53:200–213

    Google Scholar 

  89. Okanoya K, Dooling RJ (1990) Temporal integration in zebra finches (Poephila guttata). J Acoust Soc Am 87:2782–2784. https://doi.org/10.1121/1.399069

    CAS  Article  PubMed  Google Scholar 

  90. Pagel JE, Kritz KJ, Millsap BA et al (2013) Bald and golden eagle mortalities at wind energy facilities in the contiguous Unites States. J Raptor Res 47:311–315

    Article  Google Scholar 

  91. Palanca-Castan N, Laumen G, Reed D, Köppl C (2016) The binaural interaction component in barn owl (Tyto alba) presents few differences to mammalian data. J Assoc Res Otolaryngol 17:577–589. https://doi.org/10.1007/s10162-016-0583-7

    Article  PubMed  PubMed Central  Google Scholar 

  92. Parthasarathy A, Bartlett EL, Kujawa SG (2019) Age-related changes in neural coding of envelope cues: peripheral declines and central compensation. Neuroscience 407:21–31. https://doi.org/10.1016/j.neuroscience.2018.12.007

    CAS  Article  PubMed  Google Scholar 

  93. Payne RS (1971) Acoustic location of prey by barn owls (Tyto Alba). J Exp Biol 54:535–573

    CAS  PubMed  Google Scholar 

  94. Picton TW, Woods DL, Baribeau-Braun J, Healey TM (1977) Evoked potential audiometry. J Otolaryngol 6:90–119

    Google Scholar 

  95. Plantz RG, Williston JS, Jewett DL (1974) Spatio-temporal distribution of auditory-evoked far field potentials in rat and cat. Brain Res 68:55–71. https://doi.org/10.1016/0006-8993(74)90533-2

    CAS  Article  PubMed  Google Scholar 

  96. Pohl NU, Slabbekoorn H, Neubauer H et al (2013) Why longer song elements are easier to detect: threshold level-duration functions in the Great Tit and comparison with human data. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199:239–252. https://doi.org/10.1007/s00359-012-0789-z

    Article  PubMed  Google Scholar 

  97. Prum RO, Berv JS, Dornburg A et al (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–573. https://doi.org/10.1038/nature15697

    CAS  Article  PubMed  Google Scholar 

  98. Purvis A, Agapow PM, Gittleman JL, Mace GM (2000) Nonrandom extinction and the loss of evolutionary history. Science 288:328–330

    CAS  PubMed  Article  Google Scholar 

  99. Pytte CL, Ficken MS, Moiseff A (2004) Ultrasonic singing by the blue-throated hummingbird: a comparison between production and perception. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:665–673. https://doi.org/10.1007/s00359-004-0525-4

    Article  PubMed  Google Scholar 

  100. Remsen JV Jr, Areta JI, Cadena CD et al (2019) A classification of the bird species of South America. American Ornithologists’ Union. http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm. Accessed 04 Mar 2019

  101. Sachs MB, Young ED, Lewis RH (1974) Discharge patterns of single fibers in the pigeon auditory nerve. Brain Res 70:431–447

    CAS  PubMed  Article  Google Scholar 

  102. Saunders SS, Salvi RJ (1993) Psychoacoustics of normal adult chickens: thresholds and temporal integration. J Acoust Soc Am 94:83–90. https://doi.org/10.1121/1.406945

    CAS  Article  PubMed  Google Scholar 

  103. Sergeyenko Y, Lall K, Liberman MC, Kujawa SG (2013) Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci 33:13686–13694. https://doi.org/10.1523/JNEUROSCI.1783-13.2013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  104. Shaheen LA, Valero MD, Liberman MC (2015) Towards a diagnosis of cochlear neuropathy with envelope following responses. J Assoc Res Otolaryngol 16:727–745. https://doi.org/10.1007/s10162-015-0539-3

    Article  PubMed  PubMed Central  Google Scholar 

  105. Smallwood KS (2013) Comparing bird and bat fatality-rate estimates among North American wind-energy projects. Wildl Soc Bull 37:19–33. https://doi.org/10.1002/wsb.260

    Article  Google Scholar 

  106. Smallwood KS, Thelander C (2008) Bird mortality in the Altamont Pass wind resource area, California. J Wildl Manag 72:215–223

    Article  Google Scholar 

  107. Smith CA, Konishi M, Schuff N (1985) Structure of the barn owl’s (Tyto alba) inner ear. Hear Res 17:237–247

    CAS  PubMed  Article  Google Scholar 

  108. 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

    CAS  PubMed  Article  Google Scholar 

  109. Snyder RL, Schreiner CE (1984) The auditory neurophonic: basic properties. Hear Res 15:261–280

    CAS  PubMed  Article  Google Scholar 

  110. Snyder NFR, Wiley JW (1976) Sexual size dimorphism in hawks and owls of North America. Ornithol Monogr 20:1–96

    Google Scholar 

  111. Stockard JJ, Stockard JE, Sharbrough FW (1978) Nonpathologic factors influencing brainstem auditory evoked potentials. Am J EEG Technol 18:177–209

    Article  Google Scholar 

  112. Tack JD, Noon BR, Bowen ZH et al (2017) No substitute for survival: perturbation analyses using a Golden Eagle population model reveal limits to managing for take. J Raptor Res 51:258–273. https://doi.org/10.3356/JRR-16-32.1

    Article  Google Scholar 

  113. Tanaka K, Smith CA (1978) Structure of the chicken’s inner ear: SEM and TEM study. Am J Anat 153:251–271. https://doi.org/10.1002/aja.1001530206

    CAS  Article  PubMed  Google Scholar 

  114. Thiele N, Köppl C (2018) Gas anesthesia impairs peripheral auditory sensitivity in Barn Owls (Tyto alba). eNeuro. https://doi.org/10.1523/eneuro.0140-18.2018

    Article  PubMed  PubMed Central  Google Scholar 

  115. Trail PW (2017) Identifying Bald versus Golden Eagle bones: a primer for wildlife biologists and law enforcement officers. J Fish Wildl Manag 8:596–610. https://doi.org/10.3996/042017-JFWM-035

    Article  Google Scholar 

  116. Trainer JE (1946) The auditory acuity of certain birds. PhD Thesis, Cornell University

  117. US Department of Energy (DOE) (2015) Wind vision: a new era for wind power in the United States. DOE/GO-102015-4640, Washington DC

  118. US Fish and Wildlife Service (2013) Eagle conservation plan guidance. Module 1–land-based wind energy. Version 2. Division of Migratory Bird Management, Washington, DC

  119. US Fish and Wildlife Service (2016) Bald and Golden Eagles: population demographics and estimation of sustainable take in the United States, 2016 update. Division of Migratory Bird Management, Washington DC

    Google Scholar 

  120. US Government Accountability Office (GAO) (2005) Wind power: Impacts on wildlife and government responsibilities for regulating development and protecting wildlife, Report to Congressional Requesters, GAO-05-906, Washington DC

  121. van Looij MAJ, Liem S-S, van der Burg H et al (2004) Impact of conventional anesthesia on auditory brainstem responses in mice. Hear Res 193:75–82. https://doi.org/10.1016/j.heares.2004.02.009

    Article  PubMed  Google Scholar 

  122. von Békésy G (1960) Experiments in hearing. McGraw-Hill, New York

    Google Scholar 

  123. von Campenhausen M, Wagner H (2006) Influence of the facial ruff on the sound-receiving characteristics of the barn owl’s ears. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192:1073–1082. https://doi.org/10.1007/s00359-006-0139-0

    Article  Google Scholar 

  124. von Düring M, Andres KH, Simon K (1985) The comparative anatomy of the basilar papillae in birds. Fortschr Zool 30:681–685

    Google Scholar 

  125. Walsh EJ, McGee J, Javel E (1986) Development of auditory-evoked potentials in the cat. III. Wave amplitudes. J Acoust Soc Am 79:745–754

    CAS  PubMed  Article  Google Scholar 

  126. Wasser JS (1986) The relationship of energetics of falconiform birds to body mass and climate. Condor 88:57–62. https://doi.org/10.2307/1367753

    Article  Google Scholar 

  127. Watson J (2010) The Golden Eagle, 2nd edn. Bloomsbury Publishing, London

    Google Scholar 

  128. Wright TF, Schirtzinger EE, Matsumoto T et al (2008) A multilocus molecular phylogeny of the parrots (Psittaciformes): support for a Gondwanan origin during the cretaceous. Mol Biol Evol 25:2141–2156. https://doi.org/10.1093/molbev/msn160

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  129. Xia A, Liu X, Raphael PD et al (2016) Hair cell force generation does not amplify or tune vibrations within the chicken basilar papilla. Nat Commun 7:13133. https://doi.org/10.1038/ncomms13133

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  130. Young DP, Erickson WP, Strickland MD, et al (2003) Comparison of avian responses to UV-light-reflective paint on wind turbines: Subcontract Report, July 1999–December 2000. National Renewable Energy Lab., NREL/SR-500-32840, Golden

  131. Yuan Y, Shi F, Yin Y et al (2014) Ouabain-induced cochlear nerve degeneration: synaptic loss and plasticity in a mouse model of auditory neuropathy. J Assoc Res Otolaryngol 15:31–43. https://doi.org/10.1007/s10162-013-0419-7

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the essential contributions from Drs. Michelle Willette and Dana Franzen-Klein, Lori Arent, Drew Bickford, Andrew Byrne, Jamie Clark, Christopher Feist, Christopher Milliren, and The Raptor Center volunteers. This material is based upon work supported by the US Department of Energy’s Office of Energy Efficiency and Renewable Energy (EERE) under the Wind Energy—Eagle Impact Minimization Technologies and Field Testing Opportunities, Award Number DE-EE0007881.

Funding

This study was funded by the US Department of Energy’s Office of Energy Efficiency and Renewable Energy (EERE) under the Wind Energy—Eagle Impact Minimization Technologies and Field Testing Opportunities, Award Number DE-EE0007881.

Author information

Affiliations

Authors

Corresponding author

Correspondence to JoAnn McGee.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the Institutional Animal Care and Use Committee of the University of Minnesota where the studies were conducted.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Tables S1 to S6, and supplemental references (PDF 723 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

McGee, J., Nelson, P.B., Ponder, J.B. et al. Auditory performance in bald eagles and red-tailed hawks: a comparative study of hearing in diurnal raptors. J Comp Physiol A 205, 793–811 (2019). https://doi.org/10.1007/s00359-019-01367-9

Download citation

Keywords

  • Eagles
  • Hawks
  • Hearing
  • Auditory brainstem response
  • Evoked potentials