Advertisement

Journal of Comparative Physiology A

, Volume 205, Issue 4, pp 629–639 | Cite as

The paradox of hearing at the lek: auditory sensitivity increases after breeding in female gray treefrogs (Hyla chrysoscelis)

  • Alexander T. Baugh
  • Mark A. Bee
  • Megan D. GallEmail author
Original Paper

Abstract

Both behavioral receptivity and neural sensitivity to acoustic mate attraction signals vary across the reproductive cycle, particularly in seasonally breeding animals. Across a variety of taxa receptivity to signals increases, as does peripheral auditory sensitivity, as females transition from a non-breeding to breeding condition. We recently documented decreases in receptivity to acoustic mate attraction signals and circulating hormone levels, but an increase in peripheral auditory sensitivity to call-like stimuli following oviposition in Cope’s gray treefrogs (Hyla chrysoscelis). However, it is not known if changes in auditory sensitivity are confined to the frequency range of calls, or if they result from more generalized changes in the auditory periphery. Here, we used auditory brainstem responses (ABRs) to evaluate peripheral frequency sensitivity in female Cope’s gray treefrogs before and after oviposition. We found lower ABR thresholds, greater ABR amplitudes, and shorter ABR latencies following oviposition. Changes were most pronounced and consistent at lower frequencies associated with the amphibian papilla, but were also detectable at higher frequencies corresponding to the tuning of the basilar papilla. Furthermore, only ABR latencies were correlated with circulating steroid hormones (testosterone). Changes in peripheral processing may result from changes in metabolic function or sensorineural adaptation to chorus noise.

Keywords

Auditory brainstem response Corticosterone Estradiol Oviposition Testosterone 

Notes

Acknowledgements

We thank members of the Bee lab, and Jessie Tanner in particular, for assistance in collecting frogs and John Moriarty and the Three Rivers Park District for after-hours access to frog ponds.

Funding

Funding was provided by the Michener Faculty Fellowship at Swarthmore College to ATB, a National Science Foundation grant to MAB (IOS 1452831), and the Vassar College Dean of Faculty office to MDG.

Compliance with ethical standards

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 institution or practice at which the studies were conducted. Animal collections were made under Special Permit 21947 from the State of Minnesota Department of Natural Resources. This study was approved by the Institutional Animal Care and Use Committee at the University of Minnesota (Protocol 1701-34456A, approved 3 March 2017). This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

359_2019_1354_MOESM1_ESM.doc (300 kb)
Supplementary material 1 (DOC 300 kb)

References

  1. Adkins-Regan E (1998) Hormonal mechanisms of mate choice. Am Zool 38:166–178CrossRefGoogle Scholar
  2. Backus BC, Guinan JJ (2006) Time-course of the human medial olivocochlear reflex. J Acoust Soc Am 119:2889–2904CrossRefPubMedGoogle Scholar
  3. Bastien B, Farley G, Ge F, Malin JS, Simon-Plumb CL, Pulley DM, Stowell N, Yang C, Baugh AT (2018) The waiting and mating game: condition dependent mate sampling in female gray treefrogs (Hyla versicolor). Front Ecol Evol Behav Evol Ecol 6:140CrossRefGoogle Scholar
  4. Baugh AT, Bastien B, Still M, Stowell N (2018) Validation of water-borne steroid hormones in a tropical frog (Physalaemus pustulosus). Gen Comp Endocrinol 261:67–80CrossRefPubMedGoogle Scholar
  5. Beatini JR, Proudfoot GA, Gall MD (2018) Frequency sensitivity in Northern saw-whet owls (Aegolius acadicus). J Comp Physiol A 204:145–154CrossRefGoogle Scholar
  6. Bee MA (2015) Treefrogs as animal models for research on auditory scene analysis and the cocktail party problem. Int J Psychophysiol 95:216–237CrossRefPubMedGoogle Scholar
  7. Boersma P, Weenink D (2017) Praat: doing phonetics by computer [Computer program]. Version 6. 0. 29, retrieved 3 June 2018 from http://www.praat.org/
  8. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  9. Brenowitz EA (2004) Plasticity of the adult avian song control system. Ann New York Acad Sci 1016:560–585CrossRefGoogle Scholar
  10. Buerkle NP, Schrode KM, Bee MA (2014) Assessing stimulus and subject influences on auditory evoked potentials and their relation to peripheral physiology in green treefrogs (Hyla cinerea). Comp Biochem Physiol A Mol Integr Physiol 178:68–81CrossRefPubMedPubMedCentralGoogle Scholar
  11. Caras ML, Remage-Healey L (2016) Modulation of peripheral and central auditory processing by estrogens in birds. In: Bass A, Sisneros J, Popper A, Fay R (eds) Hearing and hormones. Springer handbook of auditory research, vol 57. Springer, ChamGoogle Scholar
  12. Caras ML, Brenowitz E, Rubel EW (2010) Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow. J Comp Physiol A 196:581–599CrossRefGoogle Scholar
  13. Church GT, Cudahy EA (1984) The time course of the acoustic reflex. Ear Hear 5:235–242CrossRefPubMedGoogle Scholar
  14. Cummings ME, Bernal XE, Reynaga R, Rand AS, Ryan MJ (2008) Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. J Exp Bio 211:1203–1210CrossRefGoogle Scholar
  15. Dobie RA, Humes LE (2017) Commentary on the regulatory implications of noise-induced cochlear neuropathy. Int J Audiol 56(sup1):74–78CrossRefPubMedGoogle Scholar
  16. Finneran JJ (2015) Noise-induced hearing loss in marine mammals: a review of temporary threshold shift studies from 1996 to 2015. J Acoust Soc Amer 138(3):1702–1726CrossRefGoogle Scholar
  17. Forlano PM, Sisneros JA, Rohmann KN, Bass AH (2015) Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish. Front Neuroendocrinol 37:129–145CrossRefPubMedGoogle Scholar
  18. Forlano PM, Maruska KP, Sisneros JA, Bass AH (2016) Hormone-dependent plasticity of auditory systems in fishes. In: Bass A, Sisneros J, Popper A, Fay R (eds) Hearing and hormones. Springer handbook of auditory research, vol 57. Springer, ChamGoogle Scholar
  19. Gall MD, Wilczynski W (2015) Hearing conspecific vocal signals alters peripheral auditory sensitivity. Proc R Soc B 282:20150749CrossRefPubMedGoogle Scholar
  20. Gall MD, Wilczynski W (2016) The effects of call-like masking diminish after nightly exposure to conspecific choruses in green treefrogs (Hyla cinerea). J Exp Biol 219(1295):1302Google Scholar
  21. Gall MD, Salameh TS, Lucas JR (2013) Songbird frequency selectivity and temporal resolution vary with sex and season. Proc R Soc B 280:20122296CrossRefPubMedGoogle Scholar
  22. Gall MD, Bee MA, Baugh AT (2019) The difference a day makes: breeding remodels hearing, hormones and behavior in female Cope’s gray treefrogs (Hyla chrysoscelis). Hormones Behav 108:62–72CrossRefGoogle Scholar
  23. Gerhardt HC (1975) Sound pressure levels and radiation patterns of the vocalizations of some North American frogs and toads. J Comp Physiol A 102:1–12CrossRefGoogle Scholar
  24. Gridi-Papp M, Feng AS, Shen JX, Yu ZL, Narins PM (2008) Active control of ultrasonic hearing in frogs. Proc Natl Acad Sci USA 105:11013–11018CrossRefGoogle Scholar
  25. Guinan JJ (1996) Physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds) The Cochlea. Springer handbook of auditory research, vol 8. Springer, Berlin, pp 435–502Google Scholar
  26. Guinan JJ (2006) Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 6:589–607CrossRefGoogle Scholar
  27. Hall IC, Woolley SMN, Kwong-Brown U, Kelley DB (2016) Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus). J Comp Physiol A 202:17–34CrossRefGoogle Scholar
  28. Henry KS, Lucas JR (2009) Vocally correlated seasonal auditory variation in the house sparrow (Passer domesticus). J Exp Biol 212:3817–3822CrossRefPubMedGoogle Scholar
  29. Hetherington TE (1994) The middle ear muscle of frogs does not modulate tympanic responses to sound. J Acoust Soc Am 95:2122–2125CrossRefPubMedGoogle Scholar
  30. Kelley DB (1980) Auditory and vocal nuclei in the frog brain concentrate sex hormones. Science 207:553–555CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kirk EC, Smith DW (2003) Protection from acoustic trauma is not a primary function of the medial olivocochlear efferent system. J Assoc Acoust Res 4:445–465Google Scholar
  32. Lea J, Halliday T, Dyson M (2000) Reproductive stage and history affect the phonotactic preferences of female midwife toads, Alytes muletensis. Anim Behav 60:423–427CrossRefPubMedGoogle Scholar
  33. Leary CJ (2009) Hormones and acoustic communication in anuran amphibians. Int Comp Biol 49:452–470CrossRefGoogle Scholar
  34. Lynch KS, Wilczynski W (2005) Gonadal steroid fluctuations in a tropically breeding female anuran. Gen Comp Endocrinol 43:51–56.  https://doi.org/10.1016/j.ygcen.2005.02.023 CrossRefGoogle Scholar
  35. Lynch KS, Rand AS, Ryan MJ, Wilczynski W (2005) Plasticity in female mate choice associated with changing reproductive states. Anim Behav 69:689–699CrossRefGoogle Scholar
  36. Mason MJ (2007) Pathways for sound transmission to the inner ear in amphibians. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer handbook of auditory research, vol 28. Springer, New YorkGoogle Scholar
  37. Miranda JA, Wilczynski W (2009a) Female reproductive state influences the auditory midbrain response. J Comp Physiol A 195:341–349CrossRefGoogle Scholar
  38. Miranda JA, Wilczynski W (2009b) Sex differences and androgen influences on midbrain auditory thresholds in the green treefrog, Hyla cinerea. Hear Res 252:79–88CrossRefPubMedPubMedCentralGoogle Scholar
  39. Moller AR (1974) The acoustic middle ear muscle reflex. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology, vol V/1: auditory system. Springer, Berlin, pp 519–548Google Scholar
  40. Murphy CG, Gerhardt HC (1996) Evaluating the design of mate-choice experiments: the effect of amplexus on mate choice by female barking treefrogs, Hyla gratiosa. Anim Behav 51:881–890.  https://doi.org/10.1006/anbe.1996.0092 CrossRefGoogle Scholar
  41. Nityananda V, Bee MA (2011) Finding your mate at a cocktail party: frequency separation promote auditory stream segregation of concurrent voices in multi-species frog choruses. PLoS One 6:e21191CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ophir AG, Schrader SB, Gillooly JF (2010) Energetic cost of calling: general constraints and species-specific differences. J Evol Biol 23:1564–1569CrossRefPubMedGoogle Scholar
  43. Penna M, Narins PM (1989) Effects of acoustic overstimulation on spectral and temporal processing in the amphibian auditory nerve. J Acoust Soc Am 85:1617–1629CrossRefPubMedGoogle Scholar
  44. Prestwich KN (1994) The energetics of acoustic signaling in anurans and insects. Am Zool 34:625–643CrossRefGoogle Scholar
  45. Ptacek MB, Gerhardt HC, Sage RD (1994) Speciation by polyploidy in treefrogs: multiple origins of the tetraploid, Hyla versicolor. Evolution 48:898–908CrossRefPubMedGoogle Scholar
  46. Ryan AF, Kujawa SG, Hammill T, Le Prell C, Kil J (2016) Temporary and permanent noise-induced threshold shifts: a review of basic and clinical observations. Otol Neurotol 37(8):e271–e275CrossRefPubMedPubMedCentralGoogle Scholar
  47. Salvi RJ (2008) Overview: regeneration and repair. In: Salvi RJ, Popper AN, Fay RR (eds) Hair cell regeneration, repair, and protection. Springer handbook of auditory research, vol 33. Springer, New YorkCrossRefGoogle Scholar
  48. Saunders JC, Duncan RK, Doan DE, Werner YL (2000) The middle ear of reptiles and birds. In: Dooling RJ, Fay RR, Popper AN (eds) Comparative hearing: birds and reptiles. Springer handbook of auditory research, vol 13. Springer, New YorkGoogle Scholar
  49. Schmidt AK, Riede K, Römer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762CrossRefPubMedPubMedCentralGoogle Scholar
  50. Schrode K, Ward JL, Vélez A, Bee MA (2012) Female preferences for spectral call properties in the western genetic lineage of Cope’s gray treefrog (Hyla chrysoscelis). Behav Ecol Sociobiol 66:1595–1606CrossRefPubMedPubMedCentralGoogle Scholar
  51. Schrode KM, Buerkle NP, Brittan-Powell EF, Bee MA (2014) Auditory brainstem responses in Cope’s gray treefrog (Hyla chrysocelis): effects of frequency, level, sex, and size. J Comp Physiol A 200:221–238CrossRefGoogle Scholar
  52. Schwartz JJ, Huth K, Hutchin T (2004) How long do females really listen? Assessment time for female mate choice in the grey treefrog, Hyla versicolor. Anim Behav 68:533–540CrossRefGoogle Scholar
  53. Simmons DD, Meenderink SWF, Vassilakis PN (2007) Anatomy, physiology, and function of the auditory end-organs in the frog inner ear. In: Narins PA, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians, vol 29. Springer, New York, pp 184–220Google Scholar
  54. Simmons DD, Lohr R, Wotring H, Burton MD, Hooper RA, Baird RA (2014) Recovery of otoacoustic emissions after high-level noise exposure in the American bullfrog. J Exp Biol 217:1626–1636.  https://doi.org/10.1242/jeb.090092 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305:404–407CrossRefPubMedGoogle Scholar
  56. Tanner JC, Bee MA (2018) Within-individual variation in sexual displays: signal or noise? Behav Ecol 1:2.  https://doi.org/10.1093/beheco/ary165 CrossRefGoogle Scholar
  57. Thomas RJ, Cuthill IC, Goldsmith AR, Cosgrove DF, Lidgate HC, Burdett Proctor SL (2003) The trade-off between singing and mass gain in a daytime-singing bird, the European robin. Behaviour 40:387–404CrossRefGoogle Scholar
  58. Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the neotropics. Science 214:677–678CrossRefPubMedGoogle Scholar
  59. Ward JL, Love EK, Vélez A, Buerkle NP, O’Bryan LR, Bee MA (2013) Multitasking males and multiplicative females: dynamic signaling and receiver preferences in Cope’s grey treefrog. Anim Behav 86:231–243CrossRefGoogle Scholar
  60. Wever EG (1985) The amphibian ear. Princeton University Press, PrincetonCrossRefGoogle Scholar
  61. Wilczynski W, Burmeister SS (2016) Effects of steroid hormones on hearing and communication in frogs. In: Bass A, Sisneros J, Popper A, Fay R (eds) Hearing and hormones. Springer handbook of auditory research, vol 57. Springer, ChamGoogle Scholar
  62. Witte K, Farris HE, Ryan MJ, Wilczynski W (2005) How cricket frog females deal with a noisy world: habitat-related differences in auditory tuning. Behav Ecol 16:557–571CrossRefGoogle Scholar
  63. Wong A, Gall MD (2015) Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus). Zoology 118:357–363CrossRefPubMedGoogle Scholar
  64. Zelick R, Narins PM (1985) Temporary threshold shift, adaptation, and recovery characteristics of frog auditory nerve fibers. Hear Res 17:161–176CrossRefPubMedGoogle Scholar
  65. Zhang D, Cui J, Tang Y (2012) Plasticity of peripheral auditory frequency sensitivity in Emei music frog. PLoS One 7:e45792CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Quart Rev Biol 73:415–438CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologySwarthmore CollegeSwarthmoreUSA
  2. 2.Department of Ecology, Evolution, and BehaviorUniversity of MinnesotaSt. PaulUSA
  3. 3.Graduate Program in NeuroscienceUniversity of MinnesotaMinneapolisUSA
  4. 4.Department of BiologyVassar CollegePoughkeepsieUSA

Personalised recommendations