Ear pinnae in a neotropical katydid (Orthoptera: Tettigoniidae) function as ultrasound guides for bat detection

  1. Christian A Pulver
  2. Emine Celiker
  3. Charlie Woodrow
  4. Inga Geipel
  5. Carl D Soulsbury
  6. Darron A Cullen
  7. Stephen M Rogers
  8. Daniel Veitch
  9. Fernando Montealegre-Z

  • Curated by eLife

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    Evaluation Summary:

    Remarkably, Katydids, insects related to grasshoppers and crickets, have ears in their left and right forelegs. Pulver and colleagues show convincingly how two specialized chambers lining the hearing organs function as sound resonators that effectively boost the perception of high ultrasonic frequencies. This enables Katydids to detect the echolocating pulses of their bat predators before they home in on them for a meal. This study uses an impressive combination of approaches, but the manuscript would be improved by greater clarity.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

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Abstract

Early predator detection is a key component of the predator-prey arms race and has driven the evolution of multiple animal hearing systems. Katydids (Insecta) have sophisticated ears, each consisting of paired tympana on each foreleg that receive sound both externally, through the air, and internally via a narrowing ear canal running through the leg from an acoustic spiracle on the thorax. These ears are pressure-time difference receivers capable of sensitive and accurate directional hearing across a wide frequency range. Many katydid species have cuticular pinnae which form cavities around the outer tympanal surfaces, but their function is unknown. We investigated pinnal function in the katydid Copiphora gorgonensis by combining experimental biophysics and numerical modelling using 3D ear geometries. We found that the pinnae in C. gorgonensis do not assist in directional hearing for conspecific call frequencies, but instead act as ultrasound detectors. Pinnae induced large sound pressure gains (20–30 dB) that enhanced sound detection at high ultrasonic frequencies (>60 kHz), matching the echolocation range of co-occurring insectivorous gleaning bats. These findings were supported by behavioural and neural audiograms and pinnal cavity resonances from live specimens, and comparisons with the pinnal mechanics of sympatric katydid species, which together suggest that katydid pinnae primarily evolved for the enhanced detection of predatory bats.

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  1. Version published to 10.7554/elife.77628 on eLife
  2. eLife

    Evaluation Summary:

    Remarkably, Katydids, insects related to grasshoppers and crickets, have ears in their left and right forelegs. Pulver and colleagues show convincingly how two specialized chambers lining the hearing organs function as sound resonators that effectively boost the perception of high ultrasonic frequencies. This enables Katydids to detect the echolocating pulses of their bat predators before they home in on them for a meal. This study uses an impressive combination of approaches, but the manuscript would be improved by greater clarity.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

  3. eLife

    Reviewer #1 (Public Review)

    The aim of the authors was to clarify the function of pinnae, forming part of katydid ears in the forelegs. Previous work suggested a protective function for the thin tympana or a device for directional hearing. A major strength of the paper is the combination of methods, such as experimental biophysical measurements with Laser-Doppler-Vibrometry and numerical modelling. In addition, detailed morphological data were obtained by scanning ears with a µCT-scanner, which formed the basis for producing 3D-printed models of the ear. These methods were combined with audiograms of sensory units in the ear, and measurements of behavioral sensitivity.

    Using experimental ablation of the pinnae, the authors can convincingly show that the cavities formed by the pinnae produce resonances at very high ultrasonic frequencies and that these resonances boost the perception of sound by about 20 - 30 decibels, i.e. make the ear more sensitive for these frequencies. By contrast, the data do not support the hypothesis that pinnae serve in directional hearing.

    To my knowledge, the method of performing acoustic measurements using synthetic 3D-printed scaled ear models is completely new in the field. It offers great advantages for studying the often-minute structures in insects.

  4. eLife

    Reviewer #2 (Public Review):

    In this paper, Pulver et al investigate the role of cuticular structures lining a cavity next to the tympanal ear of several Katydid grasshopper species. This hypothesis is novel and interesting and the experiments are of high quality. The combination of different experimental approaches, physical and computational models but also behavioral and neural recordings all show that the pinnae increase/allow the ability to hear high frequencies ~100 kHz. In the figures, the authors could stress their use of these different methods more.

    The results support the idea that the ear is very sensitive at 100 kHz. This coincides with the frequency content of several extant bat species.

  8. Version published to 10.1101/2021.09.01.458595v4 on bioRxiv
  9. Version published to 10.1101/2021.09.01.458595v3 on bioRxiv
  10. Version published to 10.1101/2021.09.01.458595v2 on bioRxiv
  11. Version published to 10.1101/2021.09.01.458595v1 on bioRxiv