Hearing sensitivity and amplitude coding in bats are differentially shaped by echolocation calls and social calls

Differences in auditory perception between species are influenced by phylogenetic origin and the perceptual challenges imposed by the natural environment, such as detecting prey- or predator-generated sounds and communication signals. Bats are well suited for comparative studies on auditory perception since they predominantly rely on echolocation to perceive the world, while their social calls and most environmental sounds have low frequencies. We tested if hearing sensitivity and stimulus level coding in bats differ between high and low-frequency ranges by measuring auditory brainstem responses (ABRs) of 86 bats belonging to 11 species. In most species, auditory sensitivity was equally good at both high- and low-frequency ranges, while amplitude was more finely coded for higher frequency ranges. Additionally, we conducted a phylogenetic comparative analysis by combining our ABR data with published data on 27 species. Species-specific peaks in hearing sensitivity correlated with peak frequencies of echolocation calls and pup isolation calls, suggesting that changes in hearing sensitivity evolved in response to frequency changes of echolocation and social calls. Overall, our study provides the most comprehensive comparative assessment of bat hearing capacities to date and highlights the evolutionary pressures acting on their sensory perception.

Download Full-text

Correlated evolution between hearing sensitivity and social calls in bats

Biology Letters ◽

10.1098/rsbl.2006.0501 ◽

2006 ◽

Vol 2 (4) ◽

pp. 561-564 ◽

Cited By ~ 21

Author(s):

Kirsten M Bohn ◽

Cynthia F Moss ◽

Gerald S Wilkinson

Keyword(s):

Body Size ◽

High Frequency ◽

Low Frequency ◽

Correlated Evolution ◽

Echolocation Calls ◽

Hearing Sensitivity ◽

Social Calls ◽

Frequency Components ◽

Reproductive Rates ◽

Species Specific

Echolocating bats are auditory specialists, with exquisite hearing that spans several octaves. In the ultrasonic range, bat audiograms typically show highest sensitivity in the spectral region of their species-specific echolocation calls. Well-developed hearing in the audible range has been commonly attributed to a need to detect sounds produced by prey. However, bat pups often emit isolation calls with low-frequency components that facilitate mother–young reunions. In this study, we examine whether low-frequency hearing in bats exhibits correlated evolution with (i) body size; (ii) high-frequency hearing sensitivity or (iii) pup isolation call frequency. Using published audiograms, we found that low-frequency hearing sensitivity is not dependent on body size but is related to high-frequency hearing. After controlling for high-frequency hearing, we found that low-frequency hearing exhibits correlated evolution with isolation call frequency. We infer that detection and discrimination of isolation calls have favoured enhanced low-frequency hearing because accurate parental investment is critical: bats have low reproductive rates, non-volant altricial young and must often identify their pups within large crèches.

Download Full-text

Hearing sensitivity: An underlying mechanism for niche differentiation in gleaning bats

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2024943118 ◽

2021 ◽

Vol 118 (36) ◽

pp. e2024943118 ◽

Cited By ~ 2

Author(s):

Inga Geipel ◽

Ella Z. Lattenkamp ◽

M. May Dixon ◽

Lutz Wiegrebe ◽

Rachel A. Page

Keyword(s):

Species Coexistence ◽

Ecological Factors ◽

Niche Differentiation ◽

Underlying Mechanism ◽

Auditory Brainstem ◽

Auditory Brainstem Responses ◽

Foraging Strategies ◽

Behavioral Strategies ◽

Echolocation Calls ◽

Hearing Sensitivity

Tropical ecosystems are known for high species diversity. Adaptations permitting niche differentiation enable species to coexist. Historically, research focused primarily on morphological and behavioral adaptations for foraging, roosting, and other basic ecological factors. Another important factor, however, is differences in sensory capabilities. So far, studies mainly have focused on the output of behavioral strategies of predators and their prey preference. Understanding the coexistence of different foraging strategies, however, requires understanding underlying cognitive and neural mechanisms. In this study, we investigate hearing in bats and how it shapes bat species coexistence. We present the hearing thresholds and echolocation calls of 12 different gleaning bats from the ecologically diverse Phyllostomid family. We measured their auditory brainstem responses to assess their hearing sensitivity. The audiograms of these species had similar overall shapes but differed substantially for frequencies below 9 kHz and in the frequency range of their echolocation calls. Our results suggest that differences among bats in hearing abilities contribute to the diversity in foraging strategies of gleaning bats. We argue that differences in auditory sensitivity could be important mechanisms shaping diversity in sensory niches and coexistence of species.

Download Full-text

Earless toads sense low frequencies but miss the high notes

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1670 ◽

2017 ◽

Vol 284 (1864) ◽

pp. 20171670 ◽

Cited By ~ 10

Author(s):

Molly C. Womack ◽

Jakob Christensen-Dalsgaard ◽

Luis A. Coloma ◽

Juan C. Chaparro ◽

Kim L. Hoke

Keyword(s):

High Frequency ◽

Species Differences ◽

Low Frequency ◽

Auditory Brainstem ◽

Low Frequencies ◽

Hearing Sensitivity ◽

Sensory Pathways ◽

Airborne Sound ◽

Vibrational Sensitivity ◽

Species Specific

Sensory losses or reductions are frequently attributed to relaxed selection. However, anuran species have lost tympanic middle ears many times, despite anurans' use of acoustic communication and the benefit of middle ears for hearing airborne sound. Here we determine whether pre-existing alternative sensory pathways enable anurans lacking tympanic middle ears (termed earless anurans) to hear airborne sound as well as eared species or to better sense vibrations in the environment. We used auditory brainstem recordings to compare hearing and vibrational sensitivity among 10 species (six eared, four earless) within the Neotropical true toad family (Bufonidae). We found that species lacking middle ears are less sensitive to high-frequency sounds, however, low-frequency hearing and vibrational sensitivity are equivalent between eared and earless species. Furthermore, extratympanic hearing sensitivity varies among earless species, highlighting potential species differences in extratympanic hearing mechanisms. We argue that ancestral bufonids may have sufficient extratympanic hearing and vibrational sensitivity such that earless lineages tolerated the loss of high frequency hearing sensitivity by adopting species-specific behavioural strategies to detect conspecifics, predators and prey.

Download Full-text

Auditory Brainstem Responses to Middle- and Low-Frequency Tone Pips

International Journal of Audiology ◽

10.3109/00206098409072823 ◽

1984 ◽

Vol 23 (1) ◽

pp. 75-84 ◽

Cited By ~ 24

Author(s):

M. Maurizi ◽

G. Paludetti ◽

F. Ottaviani ◽

M. Rosignoli

Keyword(s):

Low Frequency ◽

Auditory Brainstem ◽

Auditory Brainstem Responses ◽

Frequency Tone

Download Full-text

Aerial low-frequency hearing in captive and free-ranging harbour seals (Phoca vitulina) measured using auditory brainstem responses

Journal of Comparative Physiology A ◽

10.1007/s00359-016-1126-8 ◽

2016 ◽

Vol 202 (12) ◽

pp. 859-868 ◽

Cited By ~ 2

Author(s):

Klaus Lucke ◽

Gordon D. Hastie ◽

Kerstin Ternes ◽

Bernie McConnell ◽

Simon Moss ◽

...

Keyword(s):

Low Frequency ◽

Auditory Brainstem ◽

Phoca Vitulina ◽

Auditory Brainstem Responses ◽

Harbour Seals ◽

Free Ranging

Download Full-text

Auditory brainstem responses in the red-eared slider Trachemys scripta elegans (Testudoformes: Emydidae) reveal sexually dimorphic hearing sensitivity

Journal of Comparative Physiology A ◽

10.1007/s00359-019-01372-y ◽

2019 ◽

Vol 205 (6) ◽

pp. 847-854 ◽

Cited By ~ 1

Author(s):

Tongliang Wang ◽

Handong Li ◽

Jianguo Cui ◽

Xiaofei Zhai ◽

Haitao Shi ◽

...

Keyword(s):

Sexual Dimorphism ◽

Tympanic Membrane ◽

Auditory Brainstem ◽

Trachemys Scripta ◽

Auditory Brainstem Responses ◽

Sexually Dimorphic ◽

Trachemys Scripta Elegans ◽

Hearing Sensitivity ◽

Brainstem Response ◽

Auditory Systems

Abstract Hearing sensitivity is of general interest from the perspective of understanding the functionality and evolution of vertebrate auditory systems. Sexual dimorphism of auditory systems has been reported in several species of vertebrates, but little is known about this phenomenon in turtles. Some morphological characteristics, such as middle ear and tympanic membrane that influence the hearing sensitivity of animals can result in hearing sexual dimorphism. To examine whether sexual dimorphism in hearing sensitivity occurs in turtles and to compare hearing characteristics with respect to the shape of the tympanic membrane, we measured the hearing sensitivity and tympanum diameter in both sexes of Trachemys scripta elegans. The results showed that, with the exception of 0.9 kHz, auditory brainstem response thresholds were significantly lower in females than in males for frequencies in the 0.2–1.1 kHz range, indicating that the hearing of females shows greater sensitivity. No significant differences were detected in the tympanum diameter of both sexes. These results showed that sexually dimorphic hearing sensitivity has evolved in turtles; however, this difference does not appear to be related to differences in the size of the tympanic membrane. The possible origin and function of the sexual differences in auditory characteristic are discussed.

Download Full-text

Differences in Responses from the Cochleae and Central Nervous Systems of Females with Low versus High Acceptable Noise Levels

Journal of the American Academy of Audiology ◽

10.3766/jaaa.17.9.6 ◽

2006 ◽

Vol 17 (09) ◽

pp. 667-676 ◽

Cited By ~ 19

Author(s):

Ashley W. Harkrider ◽

Joanna W. Tampas

Keyword(s):

Auditory System ◽

Background Noise ◽

Otoacoustic Emissions ◽

Auditory Brainstem ◽

Auditory Brainstem Responses ◽

Intersubject Variability ◽

Hearing Sensitivity ◽

Central Regions ◽

Central Nervous Systems ◽

Medial Olivocochlear

Studies of acceptable noise level (ANL) consistently report large intersubject variability in acceptance of background noise while listening to speech. This variability is not related to age, gender, hearing sensitivity, type of background noise, speech perception in noise performance, or efferent activity of the medial olivocochlear pathway. An exploratory study was conducted to determine if differences in aggregate responses from the peripheral and central auditory system can account for intersubject variability in ANL. Click-evoked otoacoustic emissions (CEOAEs), binaural auditory brainstem responses (ABRs), and middle latency responses (MLRs) were measured in females with normal hearing with low (n = 6) versus high (n = 7) ANLs. Results of this preliminary study indicate no differences between the groups for CEOAEs or waves I or III of the ABR. Differences between the two groups emerge for the amplitudes of wave V of the ABR and for the Na-Pa component of the MLR, suggesting that physiological variations arising from more central regions of the auditory system may mediate background noise acceptance.

Download Full-text