Academic Journal
Confusion and human errors in locating synthetic frog calls: Insights into the evolution of a vocal communication signal.
| Τίτλος: | Confusion and human errors in locating synthetic frog calls: Insights into the evolution of a vocal communication signal. |
|---|---|
| Συγγραφείς: | Faizpurkar H; Biological and Life Sciences Division, School of Arts and Sciences, Ahmedabad University, Ahmedabad, Gujarat, India., Jones DL; Department of Electrical and Computer Engineering, College of Engineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA., Ratnam R; Biological and Life Sciences Division, School of Arts and Sciences, Ahmedabad University, Ahmedabad, Gujarat, India. rama.ratnam@ahduni.edu.in. |
| Πηγή: | Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology [J Comp Physiol A Neuroethol Sens Neural Behav Physiol] 2026 Sep; Vol. 212 (5), pp. 855-867. Date of Electronic Publication: 2026 May 03. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: Springer Country of Publication: Germany NLM ID: 101141792 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1351 (Electronic) Linking ISSN: 03407594 NLM ISO Abbreviation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Berlin ; New York : Springer, c2001- |
| Ιατρικοί όροι (MeSH): | Vocalization, Animal*/physiology , Anura*/physiology , Sound Localization*/physiology , Biological Evolution*, Animals ; Humans ; Acoustic Stimulation ; Male |
| Περίληψη: | Vocal communication behavior in anurans is energetically expensive and can reveal caller locations, making them vulnerable to predation. Thus, it is likely that calls have been selected to minimize energy and make signals difficult to locate. In earlier work, Jones and Ratnam (2023) suggested that differences in the acoustic receivers of anurans and mammals may be exploited to make anuran calls difficult for mammals to locate, thereby reducing some if not all predation pressure. To test some of these ideas, this study examined sound localization performance in human listeners in response to a synthetic narrowband frog call (pulsed calls of the gray treefrog Dryophytes versicolor, 28% duty-cycle) and its variations, in a dichotic listening task using interaural time differences (ITD) alone. Sounds which were easy to locate (positive control) and difficult to locate (negative control) were also tested. Localization performance in response to synthetic calls (64%) lay between those of positive control (86%) and negative control (32%, chance level). We argue that differences in performance were largely a function of call bandwidth. Among all the variations of calls that were tested (excluding controls), the synthetic call most closely resembling the gray treefrog call had the lowest call energy, the narrowest spectral bandwidth, and was the most difficult to localize. We suggest that calls may have been selected to keep their energy as low as possible by reducing their duty cycle and reducing spectral leakage to maintain narrowband characteristics. (© 2026. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.) |
| Competing Interests: | Declarations. Conflcit of interest: The authors declare no competing interests. |
| References: | Aaronson NL, Hartmann WM (2014) Testing, correcting, and extending the Woodworth model for interaural time difference. J Acoust Soc Am 135(2):817–823. https://doi.org/10.1121/1.4861243. (PMID: 10.1121/1.4861243252348903985894) Arch VS, Simmons DD, Quiñones PM, Feng AS, Jiang J, Stuart BL, Shen JX, Blair C, Narins PM (2012) Inner ear morphological correlates of ultrasonic hearing in frogs. Hear Res 283(1–2):70–79. https://doi.org/10.1016/j.heares.2011.11.006. (PMID: 10.1016/j.heares.2011.11.00622146424) Bernal XE, Stanley Rand A, Ryan MJ (2007) Sexual differences in the behavioral response of túngara frogs, Physalaemus pustulosus, to cues associated with increased predation risk. Ethology 113(8):755–763. https://doi.org/10.1111/j.1439-0310.2007.01374.x. (PMID: 10.1111/j.1439-0310.2007.01374.x) Brush JS, Narins PM (1989) Chorus dynamics of a neotropical amphibian assemblage: comparison of computer simulation and natural behaviour. Anim Behav 37:33–44. https://doi.org/10.1016/0003-3472(89)90004-3. (PMID: 10.1016/0003-3472(89)90004-3) Capranica, Robert R (1965) The Evoked Vocal Response of the Bullfrog. The MIT Press, Cambridge, Massachusetts. Christensen-Dalsgaard J (2005) Directional hearing in nonmammalian tetrapods. In: Popper AN, Fay RR (eds) Sound Source Localization. Springer, New York, pp 67–123. (PMID: 10.1007/0-387-28863-5_4) Christensen-Dalsgaard J (2011) Vertebrate pressure-gradient receivers. Hear Res 273:37–45. https://doi.org/10.1016/j.heares.2010.08.007. (PMID: 10.1016/j.heares.2010.08.00720727396) Coates MM, Narins PM (2010) Manganese-enhanced magnetic resonance imaging in the frog brain. Integr Comp Biol 50:E30–E30. Dietz M, Marquardt T, Salminen NH, McAlpine D (2013) Emphasis of spatial cues in the temporal fine structure during the rising segments of amplitude-modulated sounds. Proc Natl Acad Sci 110(37):15151–15156. https://doi.org/10.1073/pnas.1309712110. (PMID: 10.1073/pnas.1309712110239801613773782) Farahbakhsh NA, Narins PM (2006) Slow motility in hair cells of the frog amphibian papilla: Ca2+-dependent shape changes. Hear Res 212(1–2):140–159. https://doi.org/10.1016/j.heares.2005.11.004. (PMID: 10.1016/j.heares.2005.11.00416426781) Feng AS, Shofner WP (1981) Peripheral basis of sound localization in anurans. Acoustic properties of the frog’s ear. Hear Res 5:201–216. https://doi.org/10.1016/0378-5955(81)90046-0. (PMID: 10.1016/0378-5955(81)90046-06975773) Folkerts ML, Stecker GC (2022) Spectral weighting functions for lateralization and localization of complex sound. J Acoust Soc Am 151(5):3409–3425. https://doi.org/10.1121/10.0011469. (PMID: 10.1121/10.0011469356499409132592) Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press. Given MF (1988) Growth rate and the cost of calling activity in male carpenter frogs, Rana virgatipes. Behav Ecol Sociobiol 22(3):153–160. https://doi.org/10.1007/BF00300564. (PMID: 10.1007/BF00300564) Glasberg BR, Moore BC (1990) Derivation of auditory filter shapes from notched-noise data. Hear Res 47:103–138. https://doi.org/10.1016/0378-5955(87)90050-5. (PMID: 10.1016/0378-5955(87)90050-52228789) Green DM, Swets JA (1966) Signal detection theory and psychophysics. New York Wiley 1:1969–2012. https://doi.org/10.1016/0022-460X(67)90197-6. (PMID: 10.1016/0022-460X(67)90197-6) Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012. (PMID: 10.1152/physrev.00026.200920664077) Hautus MJ, Macmillan NA, Creelman CD (2021) Detection theory: A user’s guide. Routledge. https://doi.org/10.4324/9781003203636. Haywood NR, McAlpine D (2020) Estimating the perceptual weighting of interaural time difference cues in amplitude modulated binaural beats. J Acoust Soc Am 148(2):185–189. https://doi.org/10.1121/10.0001747. (PMID: 10.1121/10.0001747) Haywood NR, Undurraga JA, McAlpine D (2021) The influence of envelope shape on the lateralization of amplitude-modulated, low-frequency sound. J Acoust Soc Am 149(5):3133–3150. https://doi.org/10.1121/10.0004788. (PMID: 10.1121/10.000478834241105) Heffner RS, Heffner HE (1992) Visual factors in sound localization in mammals. J Comp Neurol 317(3):219–232. https://doi.org/10.1002/cne.903170302. (PMID: 10.1002/cne.9031703021577997) Ihlefeld A, Alamatsaz N, Shapley RM (2019) Circling back on theories of sound localization. J Acoust Soc Am 145(3_Supplement):1759–1759. https://doi.org/10.1121/1.5101438. (PMID: 10.1121/1.5101438) Jeffress LA (1948) A place theory of sound localization. J Comp Physiol Psychol 41:35–39. (PMID: 10.1037/h006149518904764) Jones DL, Ratnam R (2023) Are frog calls relatively difficult to locate by mammalian predators? J Comp Physiol A 209(1):11–30. https://doi.org/10.1007/s00359-022-01594-7. (PMID: 10.1007/s00359-022-01594-7) Lewis ER, Narins PM (1999) The acoustic periphery of amphibians: anatomy and physiology. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 101–154. (PMID: 10.1007/978-1-4612-0533-3_4) Macpherson EA, Middlebrooks JC (2002) Listener weighting of cues for lateral angle: The duplex theory of sound localization revisited. J Acoust Soc Am 111(5):219–2236. https://doi.org/10.1121/1.1471898. (PMID: 10.1121/1.1471898) Mangiamele LA, Burmeister SS (2011) Auditory selectivity for acoustic features that confer species recognition in the tungara frog. J Exp Biol 214(17):2911–2918. https://doi.org/10.1242/jeb.058362. (PMID: 10.1242/jeb.05836221832134) Markoulidakis I, Kopsiaftis G, Rallis I, Georgoulas I (2021) Multi-class confusion matrix reduction method and its application on net promoter score classification problem. In: Proceedings of the 14th Pervasive technologies related to assistive environments conference pp. 412–419. https://doi.org/10.1145/3453892.3461323. Marler P (1955) Characteristics of some animal calls. Nature 176(4470):6–8. https://doi.org/10.1038/176006a0. (PMID: 10.1038/176006a0) Mason MJ, Narins PM (2002a) Vibrometric studies of the middle ear of the bullfrog Rana catesbeiana I The extrastapes. J Exp Biol 205(20):3153–3165. https://doi.org/10.1242/jeb.205.20.3153. (PMID: 10.1242/jeb.205.20.315312235195) Mason MJ, Narins PM (2002b) Vibrometric studies of the middle ear of the bullfrog Rana catesbeiana II. The operculum. J Exp Biol 205(20):3167–3176. https://doi.org/10.1242/jeb.205.20.3167. (PMID: 10.1242/jeb.205.20.316712235196) Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42:135–159. https://doi.org/10.1146/annurev.ps.42.020191.001031. (PMID: 10.1146/annurev.ps.42.020191.0010312018391) Narins PM (2016) ICE on the road to auditory sensitivity reduction and sound localization in the frog. Biol Cybern 110(4):263–270. https://doi.org/10.1007/s00422-016-0700-z. (PMID: 10.1007/s00422-016-0700-z27699483) Narins PM, Capranica RR (1976) Sexual differences in the auditory system of the tree frog Eleutherodactylus coqui. Science 192(4237):378–380. https://doi.org/10.1126/science.1257772. (PMID: 10.1126/science.12577721257772) Narins PM, Capranica RR (1977) An automated technique for analysis of temporal features in animal vocalizations. Anim Behav 25:615–621. https://doi.org/10.1016/0003-3472(77)90112-9. (PMID: 10.1016/0003-3472(77)90112-9) Narins PM, Hödl W, Grabul DS (2003) Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. Proc Natl Acad Sci USA 100(2):577–580. https://doi.org/10.1073/pnas.0237165100. (PMID: 10.1073/pnas.023716510012515862141038) Narins PM, Evans EF, Pick GF, Wilson JP (2007) A comb-filtered noise generator for use in auditory neurophysiological and psychophysical experiments. IEEE Trans Biomed Eng BME. 26(1):43–47. (PMID: 10.1109/TBME.1979.326476) Narins PM, Lewis ER, Purgue AP, Bishop PJ, Minter LR, Lawson DP (2001) Functional consequences of a novel middle ear adaptation in the central African frog Petropedetes parkeri (Ranidae). J Exp Biol 204(7):1223–1232. https://doi.org/10.1242/jeb.204.7.1223. (PMID: 10.1242/jeb.204.7.122311249833) Narins PM (1976) Auditory Processing of Biologically Meaningful Sounds in the Treefrog, Eleutherodactylus coqui. Ph.D. thesis, Cornell University, Ithaca, New York. Peirce J, Gray JR, Simpson S, MacAskill M, Höchenberger R, Sogo H, Lindeløv JK (2019) PsychoPy2: Experiments in behavior made easy. Behav Res Methods 51(1):195–203. https://doi.org/10.3758/s13428-018-01193-y. (PMID: 10.3758/s13428-018-01193-y307342066420413) Purgue AP, Narins PM (2000) Mechanics of the inner ear of the bullfrog (Rana catesbeiana): the contact membranes and the periotic canal. J Comp Physiol A 186(5):481–488. https://doi.org/10.1007/s003590050446. (PMID: 10.1007/s00359005044610879950) Ringler E, Coates M, Cobo-Cuan A, Harris NG, Narins PM (2019) MEMRI for visualizing brain activity after auditory stimulation in frogs. Behav Neurosci 133(3):329. https://doi.org/10.1037/bne0000318. (PMID: 10.1037/bne0000318310453946600870) Risoud M, Hanson JN, Gauvrit F, Renard C, Lemesre PE, Bonne NX, Vincent C (2018) Sound source localization. Eur Ann Otorhinolaryngol Head Neck Dis 135(4):259–264. https://doi.org/10.1016/j.anorl.2018.04.009. (PMID: 10.1016/j.anorl.2018.04.00929731298) Ryan MJ, Tuttle MD, Taft LK (1981) The costs and benefits of frog chorusing behavior. Behav Ecol Sociobiol 8:273–278. https://doi.org/10.1007/BF00299526. (PMID: 10.1007/BF00299526) Ryan MJ (1985) The túngara frog: a study in sexual selection and communication. University of Chicago Press. Ryan MJ, Fox JH, Wilczynski W, Rand AS (1990) Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343(6253):66–67. https://doi.org/10.1038/343066a0. (PMID: 10.1038/343066a02296291) Simmons DD, Bertolotto C, Narins PM (1994) Morphological gradients in sensory hair cells of the amphibian papilla of the frog, Rana pipiens pipiens. Hear Res 80(1):71–78. https://doi.org/10.1016/0378-5955(94)90010-8. (PMID: 10.1016/0378-5955(94)90010-87852205) Simmons DD, Bertolotto C, Narins PM (1992) Innervation of the amphibian and basilar papillae in the leopard frog: reconstructions of single labeled fibers. J Comp Neurol 322(2):191–200. https://doi.org/10.1002/cne.903220205. (PMID: 10.1002/cne.9032202051522248) Smotherman MS, Narins PM (1999) Potassium currents in auditory hair cells of the frog basilar papilla. Hear Res 132(1–2):117–130. https://doi.org/10.1016/s0378-5955(99)00047-7. (PMID: 10.1016/s0378-5955(99)00047-710392554) Stecker GC, Bernstein LR, Brown AD (2021) Binaural hearing with temporally complex signals. In: Litovsky RY, Goupell MJ, Fay RR, Popper AN (eds) Binaural Hearing: With 93 Illustrations. Springer International Publishing, Cham, pp 145–180. Stevens SS, Newman EB (1936) The localization of actual sources of sound. Am J Psychol 48(2):297–306. https://doi.org/10.2307/1415748. (PMID: 10.2307/1415748) Tardif E, Murray MM, Meylan R, Spierer L, Clarke S (2006) The spatio-temporal brain dynamics of processing and integrating sound localization cues in humans. Brain Res 1092(1):161–176. https://doi.org/10.1016/j.brainres.2006.03.095. (PMID: 10.1016/j.brainres.2006.03.09516684510) Terhune JM (1974) Directional hearing of a harbor seal in air and water. J Acoust Soc Am 56(6):1862–1865. https://doi.org/10.1121/1.1903523. (PMID: 10.1121/1.19035234443485) Tuttle MD, Taft LK, Ryan MJ (1981) Acoustical location of calling frogs by Philander Opossums. Biotropica 13(3):233–234. https://doi.org/10.2307/2388132. (PMID: 10.2307/2388132) van Dijk P, Narins PM, Wang J (1996) Spontaneous otoacoustic emissions in seven frog species. Hear Res 101(1–2):102–112. https://doi.org/10.1016/S0378-5955(96)00140-2. (PMID: 10.1016/S0378-5955(96)00140-28951437) Wells KD, Schwartz JJ (2007) The behavioral ecology of anuran communication. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 44–86. Willi UB, Bronner GN, Narins PM (2006) Middle ear dynamics in response to seismic stimuli in the Cape golden mole (Chrysochloris asiatica). J Exp Biol 209(2):302–313. https://doi.org/10.1242/jeb.01989. (PMID: 10.1242/jeb.0198916391352) Woodworth RS, Schlosberg H (1954) Experimental psychology. Oxford and IBH Publishing. Yost WA, Zhong X (2014) Sound source localization identification accuracy: Bandwidth dependencies. J Acoust Soc Am 136(5):2737–2746. https://doi.org/10.1121/1.4898045. (PMID: 10.1121/1.489804525373973) Yost WA (2021). Sound Localization and Binaural Hearing. In: Fundamentals of Hearing: An Introduction. Leiden, The Netherlands: Brill. https://doi.org/10.1163/9789004501935_014. Zelick RD, Narins PM (1983) Intensity discrimination and the precision of call timing in two species of neotropical treefrogs. J Comp Physiol A 153:403–412. (PMID: 10.1007/BF00612594) Zelick RD, Narins PM (1985) Characterization of the advertisement call oscillator in the frog Eleutherodactylus coqui. J Comp Physiol A 156:223–229. (PMID: 10.1007/BF00610865) |
| Grant Information: | URBSASI20A5 Ahmedabad University |
| Contributed Indexing: | Keywords: Anuran vocalization; Dichotic testing; Interaural time difference; Signal detection theory; Time-frequency trade-off |
| Entry Date(s): | Date Created: 20260503 Date Completed: 20261006 Latest Revision: 20261006 |
| Update Code: | 20261007 |
| DOI: | 10.1007/s00359-026-01810-8 |
| PMID: | 42070177 |
| Βάση Δεδομένων: | MEDLINE |
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