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Unexpected dynamic up-tuning of auditory organs in day-flying moths

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Abstract

In certain nocturnal moth species the frequency range of best hearing shifts to higher frequencies during repeated sound stimulation. This could provide the moths with a mechanism to better detect approaching echolocating bats. However, such a dynamic up-tuning would be of little value for day-flying moths that use intra-specific acoustic communication. Here we examined if the ears of day-flying moths provide stable tuning during longer sound stimulation. Contrary to our expectations, dynamic up-tuning was found in the ear of the day-flying species Urania boisduvalii and Empyreuma pugione. Audiograms were measured with distortion-product otoacoustic emissions (DPOAEs). The level of the dominant distortion product (i.e. 2f1–f2) varied as a function of time by as much as 45 dB during ongoing acoustic stimulation, showing a systematic decrease at low frequencies and an increase at high frequencies. As a consequence, within about 2 s of acoustic stimulation, the DPOAEs audiogram shifted from low to high frequencies. Despite the up-tuning, the range of best audition still fell within the frequency band of the species-specific communication signals, suggesting that intra-specific communication should not be affected adversely. Up-tuning could be an ancestral condition in moth ears that in day-flying moths does not underlie larger selection pressure.

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Abbreviations

DP:

Distortion products

DPOAEs:

Distortion-product otoacoustic emissions

FFT:

Fast Fourier transform

LVD:

Laser Doppler vibrometry

SPL:

Sound pressure level

References

  • Adams WB (1972) Mechanical tuning of the acoustic receptor of Prodenia eridania (Cramer) (Noctuidae). J Exp Biol 57:297–304

    Google Scholar 

  • Asi NS, Fullard JH, Whitehead S, Dawson JW (2009) No neural evidence for dynamic auditory tuning of the A1 receptor in the ear of the noctuid moth, Noctua pronuba. J Comp Physiol A 195:955–960. doi:10.1007/s00359-009-0471-2

    Article  CAS  Google Scholar 

  • Barro A, Vater M, Pérez M, Coro F (2009) Surface structure of sound emission organs in Urania moths. In: Gorb SN (ed) Functional surfaces in biology. Springer, pp 189–199

  • Bergevin C, Freeman DM, Saunders JC, Shera CA (2008) Otoacoustic emissions in humans, birds, lizards, and frogs: evidence for multiple generation mechanisms. J Comp Physiol A 194:665–683

    Article  Google Scholar 

  • Boyev KP, Liberman MC, Brown MC (2002) Effects of anesthesia on efferent-mediated adaptation of the DPOAE. J Acoust Soc Am 3:362–373. doi:10.1007/s101620020044

    CAS  Google Scholar 

  • Conner WE (1999) ‘Un chant d’appel amoureux’: acoustic communication in moths. J Exp Biol 202:1711–1723

    PubMed  Google Scholar 

  • Conner WE, Corcoran AJ (2012) Sound strategies: the 65-million-year-old battle between bats and insects. Ann Rev Entomol 57:21–39. doi:10.1146/annurev-ento-121510-133537

    Article  CAS  Google Scholar 

  • Coro F (1986) El órgano timpánico de Urania boisduvalii (Lepidoptera: Uraniidae). Cien Biol 15:3–17

    Google Scholar 

  • Coro F, Kössl M (1998) Distortion-product otoacoustic emissions from the tympanic organ in two noctuoid moths. J Comp Physiol A 183:525–531. doi:10.1007/s003590050278

    Article  Google Scholar 

  • Coro F, Kössl M (2001) Components of the 2f(1)–f(2) distortion-product otoacoustic emission in a moth. Hear Res 162:126–133

    Article  CAS  PubMed  Google Scholar 

  • Fenton MB, Fullard JH (1979) Influence of moth hearing on bat echolocation strategies. J Comp Physiol A 132:77–86

    Article  Google Scholar 

  • Fernández Y, Pérez M, Mora EC (2013) Is accoustic communication essential in the mating behavior of Empyreuma pugione (Erebidae: Arctiinae)? Revista Cubana de Ciencias Biológicas 2:32–37

    Google Scholar 

  • Fournier JP, Dawson JW, Mikhail A, Yack JE (2013) If a bird flies in the forest, does an insect hear it? Biol Lett 9:20130319. doi:10.1098/rsbl.2013.0319

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fullard JH (1988) The tuning of moth ears. Experientia 44:423–428

    Article  Google Scholar 

  • Fullard JH (1994) Auditory changes in noctuid moths endemic to a bat-free habitat. J Evol Biol 7:435–445

    Article  Google Scholar 

  • Fullard JH (1998) The sensory coevolution of moths and bats. In: Hoy R, Popper A, Fay R (eds) Comparative hearing: insects. Springer-Verlag, New York, pp 279–326

    Chapter  Google Scholar 

  • Fullard JH (2006) Evolution of hearing in moths: the ears of Oenosandra boisduvalii (Noctuoidea: Oenosandridae). Aust J Zool 54:51–56. doi:10.1071/Zo05066

    Article  Google Scholar 

  • Fullard JH, Dawson JW (1999) Why do diurnal moths have ears? Naturwissenschaften 86:276–279

    Article  CAS  Google Scholar 

  • Fullard JH, Napoleone N (2001) Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera. Anim Behav 62:349–368. doi:10.1006/anbe.2001.1753

    Article  Google Scholar 

  • Fullard JH, Dawson JW, Otero LD, Surlykke A (1997) Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae). J Comp Physiol A 181:477–483

    Article  CAS  PubMed  Google Scholar 

  • Fullard JH, Otero LD, Orellana A, Surlykke A (2000) Auditory sensitivity and diel flight activity in neotropical Lepidoptera. Ann Entomol Soc Am 93:956–965. doi:10.1603/0013-8746(2000)093[0956:ASADFA]2.0.Co;2

  • Goerlitz HR, ter Hofstede HM, Zeale MRK, Jones G, Holderied MW (2010) An aerial-hawking bat uses stealth echolocation to counter moth hearing. Curr Biol 20:1568–1572. doi:10.1016/j.cub.2010.08.057

    Article  CAS  PubMed  Google Scholar 

  • Halsey K, Skjonsberg A, Ulfendahl M, Dolan DF (2005) Efferent-mediated adaptation of the DPOAE as a predictor of aminoglycoside toxicity. Hear Res 201:99–108. doi:10.1016/j.heares.2004.09.010

    Article  CAS  PubMed  Google Scholar 

  • Jacobs DS, Ratcliffe JM, Fullard JH (2008) Beware of bats, beware of birds: the auditory responses of eared moths to bat and bird predation. Behav Ecol 19:1333–1342. doi:10.1093/beheco/arn071

    Article  Google Scholar 

  • Kim DO, Dorn PA, Neely ST, Gorga MP (2001) Adaptation of distortion product otoacoustic emission in humans. J Acoust Soc Am 2:31–40. doi:10.1007/s101620010066

    CAS  Google Scholar 

  • Kössl M, Coro F (2006) L1, L2 maps of distortion-product otoacoustic emissions from a moth ear with only two auditory receptor neurons. J Acoust Soc Am 120:3822–3831

    Article  PubMed  Google Scholar 

  • Kössl M, Coro F, Seyfarth EA, Nassig WA (2007) Otoacoustic emissions from insect ears having just one auditory neuron. J Comp Physiol A 193:909–915. doi:10.1007/s00359-007-0244-8

    Article  Google Scholar 

  • Kössl M, Mockel D, Weber M, Seyfarth EA (2008) Otoacoustic emissions from insect ears: evidence of active hearing? J Comp Physiol A 194:597–609. doi:10.1007/s00359-008-0344-0

    Article  Google Scholar 

  • Kujawa SG, Liberman MC (2001) Effects of olivocochlear feedback on distortion product otoacoustic emissions in guinea pig. J Acoust Soc Am 2:268–278. doi:10.1007/s101620010047

    CAS  Google Scholar 

  • Lees DC (1992) Foreleg stridulation in male Urania moths (Lepidoptera: Uraniidae). Zool J Linn Soc 106:163–170. doi:10.1111/j.1096-3642.1992.tb01245.x

    Article  Google Scholar 

  • Liberman MC, Puria S, Guinan JJ (1996) The ipsilaterally evoked olivocochlear reflex causes rapid adaptation of the 2f1–f2 distortion product otoacoustic emission. J Acoust Soc Am 99:3572–3584. doi:10.1121/1.414956

    Article  CAS  PubMed  Google Scholar 

  • Luebke AE, Foster PK, Stagner BB (2002) A multifrequency method for determining cochlear efferent activity. J Acoust Soc Am 3:16–25. doi:10.1007/s101620010089

    Google Scholar 

  • Meinke DK, Stagner BB, Martin GK, Lonsbury-Martin BL (2005) Human efferent adaptation of DPOAEs in the L1, L2 space. Hear Res 208:89–100. doi:10.1016/j.heares.2005.05.004

    Article  PubMed  Google Scholar 

  • Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51:570–581

    Article  Google Scholar 

  • Möckel D, Seyfarth EA, Kössl M (2007) The generation of DPOAEs in the locust ear is contingent upon the sensory neurons. J Comp Physiol A 193:871–879. doi:10.1007/s00359-007-0239-5

    Article  Google Scholar 

  • Möckel D, Seyfarth EA, Kössl M (2011) Otoacoustic emissions in bushcricket ears: general characteristics and the influence of the neuroactive insecticide pymetrozine. J Comp Physiol A 197:193–202. doi:10.1007/s00359-010-0599-0

    Article  Google Scholar 

  • Möckel D, Nowotny M, Kössl M (2014) Mechanical basis of otoacoustic emissions in tympanal hearing organs. J Comp Physiol A 200:681–691

    Article  Google Scholar 

  • Mora EC, Macías S, Vater M, Coro F, Kössl M (2004) Specializations for aerial hawking in the echolocation system of Molossus molossus (Molossidae, Chiroptera). J Comp Physiol A 190:561–574

    Article  CAS  Google Scholar 

  • Mora EC, Cobo-Cuan A, Macias-Escriva F, Perez M, Nowotny M, Kössl M (2013) Mechanical tuning of the moth ear: distortion-product otoacoustic emissions and tympanal vibrations. J Exp Biol 216:3863–3872. doi:10.1242/jeb.085902

    Article  PubMed  Google Scholar 

  • Nakano R et al (2008) Moths produce extremely quiet ultrasonic courtship songs by rubbing specialized scales. Proc Natl Acad Sci USA 105:11812–11817. doi:10.1073/pnas.0804056105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pérez Álvarez M, Barro A (2014) Functional characteristics of the tympanic organ of Urania boisduvalii (Lepidoptera: Geometroidea: Uraniidae) and its behavioral role. Revista Cubana de Ciencias Biológicas 3:81–94

    Google Scholar 

  • Rydell J, Jones G, Waters D (1995) Echolocating bats and hearing moths: who are the winners? Oikos 73:419–424

    Article  Google Scholar 

  • Sanderford M, Coro F, Conner W (1998) Courtship behavior in Empyreuma affinis Roths (Lepidoptera, Arctiidae, Ctenuchinae): acoustic signals and tympanic organ response. Naturwissenschaften 85:82–87

    Article  CAS  Google Scholar 

  • Schlenther D, Voss C, Kössl M (2014) Influence of ketamine–xylazine anaesthesia on cubic and quadratic high-frequency distortion-product otoacoustic emissions. JARO 15:695–705

    Article  CAS  PubMed  Google Scholar 

  • Schnitzler H-U, Kalko EK (2001) Echolocation by insect-eating bats. Bioscience 51:557–569

    Article  Google Scholar 

  • StatSoft Inc. (2001) STATISTICA for Windows 6.0. Statsoft Inc., Tulsa, Oklahoma

  • Sun XM, Kim DO (1999) Adaptation of 2f1–2f2 distortion product otoacoustic emission in young-adult and old CBA and C57 mice. J Acoust Soc Am 105:3399–3409. doi:10.1121/1.424668

    Article  CAS  PubMed  Google Scholar 

  • Surlykke A, Fullard JH (1989) Hearing of the Australian whistling moth, Hecatesia thyridion. Naturwissenschaften 76:132–134. doi:10.1007/Bf00366610

    Article  Google Scholar 

  • Surlykke A, Skals N, Rydell J, Svensson M (1998) Sonic hearing in a diurnal geometrid moth, Archiearis parthenias, temporally isolated from bats. Naturwissenschaften 85:36–37. doi:10.1007/s001140050449

    Article  CAS  Google Scholar 

  • Takanashi T, Nakano R, Surlykke A, Tatsuta H, Tabata J, Ishikawa Y, Skals N (2010) Variation in courtship ultrasounds of three Ostrinia moths with different sex pheromones. PloS One 5. doi:10.1371/journal.pone.0013144

  • Windmill JF, Jackson JC, Tuck EJ, Robert D (2006) Keeping up with bats: dynamic auditory tuning in a moth. Curr Biol 16:2418–2423. doi:10.1016/j.cub.2006.09.066

    Article  CAS  PubMed  Google Scholar 

  • Yack JE, Fullard JH (2000) Ultrasonic hearing in nocturnal butterflies. Nature 403:265–266

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank students at Havana University for collecting animals in the field. We thank the three anonymous reviewers for their helpful comments. This work was supported by the Institute Partnership Stipendium from the Alexander von Humboldt Foundation to the Research Groups of ECM and MK. Capture, holding and experimental procedures used in this study were approved by the animal care committees of the University of Frankfurt and University of Havana.

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The authors declare that they have no conflict of interest.

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Correspondence to Emanuel C. Mora.

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Emanuel C. Mora and Ariadna Cobo-Cuan are equal first authors.

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Mora, E.C., Cobo-Cuan, A., Macías-Escrivá, F. et al. Unexpected dynamic up-tuning of auditory organs in day-flying moths. J Comp Physiol A 201, 657–666 (2015). https://doi.org/10.1007/s00359-015-1009-4

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