The Science of Nature

, 102:43 | Cite as

The unique sound production of the Death’s-head hawkmoth (Acherontia atropos (Linnaeus, 1758)) revisited

  • Gunnar Brehm
  • Martin Fischer
  • Stanislav Gorb
  • Thomas Kleinteich
  • Bernhard Kühn
  • David Neubert
  • Hans Pohl
  • Benjamin Wipfler
  • Susanne Wurdinger
Original Paper

Abstract

When disturbed, adults of the Death’s-head hawkmoth (Lepidoptera, Sphingidae: Acherontia atropos) produce short squeaks by drawing in and deflating air into and out of the pharynx as a defence mechanism. We took a new look at Prell’s hypothesis of a two-phase mechanism by providing new insights into the functional morphology behind the pharyngeal sound production of this species. First, we compared the head anatomy of A. atropos with another sphingid species, Manduca sexta, by using micro-computed tomography (CT) and 3D reconstruction methods. Despite differences in feeding behaviour and capability of sound production in the two species, the musculature in the head is surprisingly similar. However, A. atropos has a much shorter proboscis and a modified epipharynx with a distinct sclerotised lobe projecting into the opening of the pharynx. Second, we observed the sound production in vivo with X-ray videography, mammography CT and high-speed videography. Third, we analysed acoustic pressure over time and spectral frequency composition of six A. atropos specimens, both intact and with a removed proboscis. Single squeaks of A. atropos last for ca. 200 ms and consist of an inflation phase, a short pause and a deflation phase. The inflation phase is characterised by a burst of ca. 50 pulses with decreasing pulse frequency and a major frequency peak at ca. 8 kHz, followed by harmonics ranging up to more than 60 kHz. The deflation phase is characterised by a less clear acoustic pattern, a lower amplitude and more pronounced peaks in the same frequency range. The removal of the proboscis resulted in a significantly shortened squeak, a lower acoustic pressure level and a slightly more limited frequency spectrum. We hypothesise that the uptake of viscous honey facilitated the evolution of an efficient valve at the opening of the pharynx (i.e. a modified epipharynx), and that sound production could relatively easily have evolved based on this morphological pre-adaptation.

Keywords

Insect anatomy Insect head Proboscis Manduca sexta X-ray imaging Insect acoustics Videography 

Notes

Acknowledgments

Work on Acherontia sound was inspired by the special exhibition ‘Falten in Natur und Technik’ in the Phyletisches Museum, Friedrich-Schiller Universität Jena (2014–2015) of which it was also a part. We thank Ian Kitching (Natural History Museum, London) and Wolfgang Nässig (Senckenberg Museum, Frankfurt) for the suggestions on the literature, Stefan Franke (Ernst-Abbe-Hochschule, Jena) for supporting the acoustic analyses, Rainer Plontke (Magdala) for organising the Acherontia specimens, Sandra Niederschuh (Jena) for an introduction to the Photron camera system, Markus Knaden and Sylke Dietel-Gläßer (Max Planck Institute for Chemical Ecology, Jena) for providing the M. sexta specimens, Marion Schrumpf (Max Planck Institute for Biogeochemistry, Jena) for help in producing Fig. 2, Vicky Kastner (Tübingen) for the linguistic improvement of the manuscript and Esther Appel (Kiel) for the critical point drying of A. atropos. Comments by four anonymous reviewers significantly helped to improve our manuscript. TK (grant KL2707/2-1) and BW (grant WI4324/1-1) are supported by the DFG.

Supplementary material

ESM 1

A film (10 s length) of a manually stimulated specimen displaying a typical movement of the abdomen and squeaking three times (several days old specimen) (MP4 19042 kb)

114_2015_1292_MOESM2_ESM.wav (553 kb)
A sound file (4 s length) with a series of 19 consecutive squeaks after manual stimulation (freshly hatched specimen) (WAV 552 kb)
114_2015_1292_MOESM3_ESM.mov (2.6 mb)
A film (3.75 s length) of a consecutive series of 15 mammography X-ray images recorded at 4 frames s−1. The rapid expansion and collapse of the pharynx is visible (MOV 2687 kb)
114_2015_1292_MOESM4_ESM.mov (30.6 mb)
The compilation of a film (total: 9 min 14 s length) of a specimen in a micro CT, recorded at 1.83 frames s−1. The specimen was electrically stimulated every ca. 60 s. A reaction was visible after stimulation 1, 6, 7 and 8. Stimulation 1 and 6: The pharynx rapidly inflates and deflates. Stimulation 7: the pharynx is inflated and remains semi-inflated until stimulation 8. Note that further reactions could easily have been missed because of the low time resolution (MOV 31370 kb)
114_2015_1292_MOESM5_ESM.mp4 (14.5 mb)
A film (1.38 s length) recorded at 2000 frames s−1. Start at 1863 ms with closed mouth, mouth opens at 1913–1970 ms, stimulus is given at ca. 2650 ms, visible reaction after electric stimulation starts at 2660 ms, head is moved upwards, (air is drawn in), hemolymph fluid visible (air is deflated) from ca. 2820 ms. Stop at 3240 ms. Time between stimulus and visible deflation is thus ca. 170 ms (MP4 14835 kb)
114_2015_1292_MOESM6_ESM.xls (40 kb)
ESM 2 Overview measurements and results (XLS 39 kb)
114_2015_1292_MOESM7_ESM.csv (26.7 mb)
Sound pressure measurements part 1(CSV 27330 kb)
114_2015_1292_MOESM8_ESM.csv (5.7 mb)
Sound pressure measurements part 2(CSV 5804 kb)
114_2015_1292_MOESM9_ESM.docx (1.6 mb)
Plots sound pressure (DOCX 1658 kb)
114_2015_1292_MOESM10_ESM.docx (1.5 mb)
Additional measurements 2015 (DOCX 1552 kb)
114_2015_1292_MOESM11_ESM.pdf (169 kb)
FFT 3D plot up to 25 kHz (PDF 169 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Gunnar Brehm
    • 1
  • Martin Fischer
    • 2
  • Stanislav Gorb
    • 3
  • Thomas Kleinteich
    • 3
  • Bernhard Kühn
    • 2
  • David Neubert
    • 1
  • Hans Pohl
    • 1
  • Benjamin Wipfler
    • 1
  • Susanne Wurdinger
    • 4
  1. 1.Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem MuseumFriedrich-Schiller-Universität JenaJenaGermany
  2. 2.Ernst-Abbe-Hochschule JenaJenaGermany
  3. 3.Functional Morphology and BiomechanicsKiel UniversityKielGermany
  4. 4.Universitätsklinikum JenaJenaGermany

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