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.
Similar content being viewed by others
Notes
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.
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
American Wind Energy Association (AWEA) (2018) U.S. wind industry fourth quarter 2018 market report. http://www.awea.org/2018marketreports. Accessed 04 Mar 2019
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
Barton L, Bailey ED, Gatehouse RW (1984) Audibility curve of bobwhite quail (Colinus virginianus). J Aud Res 24:87–97
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
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
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
Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 112:999–1008
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
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
Burkard R (1991) Effects of noiseburst rise time and level on the gerbil brainstem auditory evoked response. Audiology 30:47–58
Calford MB (1988) Constraints on the coding of sound frequency imposed by the avian interaural canal. J Comp Physiol A 162:491–502
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
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
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
Chen L, Salvi R, Shero M (1994) Cochlear frequency-place map in adult chickens: intracellular biocytin labeling. Hear Res 81:130–136
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
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
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
Counter SA (1985) Brain-stem evoked potentials and noise effects in seagulls. Comp Biochem Physiol A Comp Physiol 81:837–845
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
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
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
Dmitrieva LP, Gottlieb G (1992) Development of brainstem auditory pathway in mallard duck embryos and hatchlings. J Comp Physiol A 171:665–671
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
Dooling RJ (1979) Temporal summation of pure tones in birds. J Acoust Soc Am 65:1058–1060. https://doi.org/10.1121/1.382576
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
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
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
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
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
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
Fischer FP (1994) Quantitative TEM analysis of the barn owl basilar papilla. Hear Res 73:1–15
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
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
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
Garvin JC, Jennelle CS, Drake D, Grodsky SM (2011) Response of raptors to a windfarm. J Appl Ecol 48:199–209
Gill F, Donsker D (eds) (2019) IOC World Bird List (v9.1). https://doi.org/10.14344/ioc.ml.9.1
Gleich O (1989) Auditory primary afferents in the starling: correlation of function and morphology. Hear Res 37:255–267
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
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
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
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
Grandori F (1986) Field analysis of auditory evoked brainstem potentials. Hear Res 21:51–58
Grier JW (1982) Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 218:1232–1235
Gummer AW, Smolders JW, Klinke R (1987) Basilar membrane motion in the pigeon measured with the Mössbauer technique. Hear Res 29:63–92
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
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
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
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
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
Henry KR (1995) Auditory nerve neurophonic recorded from the round window of the Mongolian gerbil. Hear Res 90:176–184
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
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
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
IUCN (2019) The IUCN Red List of Threatened Species. Version 2019-1. http://www.iucnredlist.org. Accessed 21 Mar 2019
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
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
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
Jewett DL, Romano MN, Williston JS (1970) Human auditory evoked potentials: possible brain stem components detected on the scalp. Science 167:1517–1518
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
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
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
Klump GM, Kretzschmar E, Curio E (1986) The hearing of an avian predator and its avian prey. Behav Ecol Sociobiol 18:317–323
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
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
Köppl C (1997) Number and axon calibres of cochlear afferents in the barn owl. Aud Neurosci 3:313–334
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
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
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
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
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
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
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
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
Langemann U, Hamann I, Friebe A (1999) A behavioral test of presbycusis in the bird auditory system. Hear Res 137:68–76
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
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
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
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
Madders M, Whitfield DP (2006) Upland raptors and the assessment of wind farm impacts. Ibis 148:43–56
Manley GA, Köppl C (1998) Phylogenetic development of the cochlea and its innervation. Curr Opin Neurobiol 8:468–474
Manley GA, Brix J, Kaiser A (1987) Developmental stability of the tonotopic organization of the chick’s basilar papilla. Science 237:655–656
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
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
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
Mayr E (1946) The number of species of birds. Auk 63:64–69
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
Mlíkovský J (1989) Brain size in birds: 2. Falconiformes through Gaviiformes. Vést cs Spolec Zool 53:200–213
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
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
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
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
Payne RS (1971) Acoustic location of prey by barn owls (Tyto Alba). J Exp Biol 54:535–573
Picton TW, Woods DL, Baribeau-Braun J, Healey TM (1977) Evoked potential audiometry. J Otolaryngol 6:90–119
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
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
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
Purvis A, Agapow PM, Gittleman JL, Mace GM (2000) Nonrandom extinction and the loss of evolutionary history. Science 288:328–330
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
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
Sachs MB, Young ED, Lewis RH (1974) Discharge patterns of single fibers in the pigeon auditory nerve. Brain Res 70:431–447
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
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
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
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
Smallwood KS, Thelander C (2008) Bird mortality in the Altamont Pass wind resource area, California. J Wildl Manag 72:215–223
Smith CA, Konishi M, Schuff N (1985) Structure of the barn owl’s (Tyto alba) inner ear. Hear Res 17:237–247
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
Snyder RL, Schreiner CE (1984) The auditory neurophonic: basic properties. Hear Res 15:261–280
Snyder NFR, Wiley JW (1976) Sexual size dimorphism in hawks and owls of North America. Ornithol Monogr 20:1–96
Stockard JJ, Stockard JE, Sharbrough FW (1978) Nonpathologic factors influencing brainstem auditory evoked potentials. Am J EEG Technol 18:177–209
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
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
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
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
Trainer JE (1946) The auditory acuity of certain birds. PhD Thesis, Cornell University
US Department of Energy (DOE) (2015) Wind vision: a new era for wind power in the United States. DOE/GO-102015-4640, Washington DC
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
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
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
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
von Békésy G (1960) Experiments in hearing. McGraw-Hill, New York
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
von Düring M, Andres KH, Simon K (1985) The comparative anatomy of the basilar papillae in birds. Fortschr Zool 30:681–685
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
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
Watson J (2010) The Golden Eagle, 2nd edn. Bloomsbury Publishing, London
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
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
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
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
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
Authors and Affiliations
Corresponding author
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.
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-019-01367-9