Virtual Issue: Sound Production Mechanisms in Animals

1 09 2014

Elodie F. Briefer

Institute of Agricultural Sciences, ETH Zürich, Universitätstrasse 2, 8092 Zürich, Switzerland

Journal of Zoology Virtual IssueAcoustic communication is used by Arthropodes and Vertebrates, and particularly in species that move in the three-dimensional space (e.g. underwater or in forests), in order to communicate at both short and long distances. This mode of communication is highly developed in social species, and plays a crucial role in reproduction, parent-offspring communication, predator avoidance, territoriality, foraging and group communication. The modes of production of sounds and the structures used in sound production are very diverse and range from vibration of the wings in fruit flies (Drosophila) to stridulation in crickets, snapping of the swimbladder in fish, tongue clicks in some bats and vibration of the tympaniform membranes in birds or of the vocal cords in mammals. Several seminal papers on the modes of acoustic production and its link with the acoustic structure of vocalisations, as well as on the information content of vocalisations, have been published in Journal of Zoology. This free Virtual Issue gathers a selection of reviews and research papers, from various years, on the topic of sound production mechanisms in animals.

In the first selected paper, Parmentier et al. (2008) compared the structures involved in acoustic communication in three species of pearlfish (Carapidae; Carapus boraborensis, Encheliophis gracilis and Carapus homei). These small eel-like fish produce species-specific sounds that differ in temporal parameters, spectral frequencies, and sound intensity. In these species, sounds are produced through the swimbladder. The contraction of primary sonic muscles pulls the anterior bladder. When releasing the tension, the swimbladder snaps back to its resting position, producing sound. The authors analysed the sound production system as well as the acoustic features of the sounds produced. They were able to relate each part of the sounds to the action of swimbladder muscles. They also showed anatomical as well as acoustic differences between the three studied species.

With the second and third paper selected for this Virtual Issue, we move on to bird sound production. These two papers, by Thorpe (1958) and Warner (1972), are among the earliest detailed papers on the topic of sound production mechanism in birds. Thorpe (1958) is a review paper describing the vocal apparatus of birds and comparing it with human vocal apparatus. Both bird vocalisation and human voice are produced by the vibration of membranes during the exhalant phase of respiration (tympaniform membranes and vocal cords, respectively). This sound is then shaped in the resonance cavities (vocal tract above the syrinx and larynx, respectively). Warner (1972), after a historical review of previous work conducted on sound production mechanism in birds, compared the anatomy of the syrinx in several passerines birds (songbirds). His main finding is that the only demonstrable vibratile areas, hence the only sound sources, in the syrinx are the internal tympaniform membranes. These membranes, located one in each bronchus, can vibrate independently of each other, thus producing two harmonically unrelated tones at the same time (biphonation). These findings would be confirmed later on by many other studies.

Most bats produce echolocation signals, ranging from 20 to 200 kilohertz in frequency, using their larynx. However, some variation exists. For instance, a few species click their tongue, whereas horseshoe and leaf-nosed bats emit their echolocation calls through their nostrils, which are surrounded by a fleshy, horseshoe/leaf-like structure. In the fourth paper of this Virtual Issue, Robinson (1996) investigated the function of the noseleaf of horseshoe and leaf-nosed bats in echolocation. The author measured the echolocation frequency, noseleaf width, and forearm length of 14 species from the genera Rhinolophus and Hipposideros. This study revealed that noseleaf width is related to the wavelength of the echolocation signal, but not to forearm length. This suggests that noseleaf width is determined by wavelength rather than body size, thus highlighting the function of noseleaf in the production of echolocation signals.

The next paper selected for this Virtual Issue, by Sissom et al. (1991), investigates purring in cats. The mechanisms of cat purring have turned out to be challenging to understand. Indeed, the very low fundamental frequency of purring, notably in domestic cats (around 25 Hertz), suggests alternative mechanisms of sound production than flow-induced vocal cord vibration, as only very long cords could produce such low frequency. Proposed mechanisms include aerodynamic and hemodynamic vibration of the true and false vocal chords, the soft palate, and the arterial system, or muscular vibrations of the diaphragm and a repetitive closing of the glottis. The authors recorded domestic cats in a shelter and found that purring occurs during the entire respiratory cycle, with a fundamental frequency ranging between 23 and 31 Hertz. This frequency is higher during expiration than inspiration, but is quite stable throughout the life of an individual, and is not related to its weight or sex. Their results support the laryngeal mechanism but argue against the mechanical involvement of the diaphragm and intercostal muscles. Thus, purring could arise from the gating of respiratory flow by the larynx. This had been suggested also by Remmers and Gautier (1972), who showed that purring is in fact produced by active contractions of laryngeal muscles modulating the respiratory air flow passing through the vocal cords, as opposed to flow-induced self-sustaining oscillations found, for example, in humans.

According to the source-filter theory of voice production (Fant, 1960; Titze, 1994), the air flow coming from the lungs induces the oscillation of the vocal cords, thus producing the “source” sound. This sound is then filtered in the vocal tract (“filter”). Some frequencies, which correspond to the resonances of the vocal tract, will be amplified and other frequencies will be dampened. The source determines the lowest frequency of the voice (fundamental frequency) and its harmonics, while the filter determines the spectral peaks, called “formants”. In human voice, the pattern of the first two formants allows to distinguish between different vowels and is thus the basis of human speech. The source-filter theory framework has been recently adapted to other animals. The sixth paper of this Virtual Issue, by Taylor and Reby (2010), describes how mammal communication research benefited from this framework. By linking the structure of vocalizations to their mode of production, researchers have been able to highlight information, in vocalisations, about the sender’s body size, age, sex, hormonal levels, dominance status and even motivational or emotional state. This review paper describes the source-filter theory in details and the indices that are generated at the source and at the filter. The seventh paper of the Virtual Issue, by Briefer (2012), describes in more details how motivational or emotional states can affect vocalisations in humans and other mammals. In this paper, I reviewed the existing literature on vocal correlates of emotions in several mammals, in order to highlight common patterns of changes in vocal parameters and find the best source- and filter-related parameters that can reliably indicate the two main dimensions of emotions (arousal and valence).

The eighth paper selected for this Virtual Issue, by Fitch (1999), shows how the source-filter theory framework can be applied to birds, in order to explain the evolution of trachea elongation. More than 60 bird species possess an elongated trachea. Formant frequencies depend on the vocal tract length and shape, with lower frequencies indicating longer vocal tracts. Normally, the vocal tract is constrained by surrounding bones, so that its length strongly depends on body size. Formants are thus good indicators of body size in many species. However, some species possess either a mobile larynx that they can retract to lengthen the vocal tract during vocalisations (e.g. red deer and fallow deer), or possess an elongated vocal tract. Fitch suggests that these characteristics evolved through sexual selection to exaggerate perceived body size, as animals can produce vocalisations with lower formants than expected from their body size.

The ninth paper selected for this Virtual Issue investigated the source of vocal production in muskoxen (Ovibos moschatus), a large ungulate of the family Bovidae and subfamily Caprinae. Although highly sexually dimorphic (males are 1/3 heavier than females), both sexes of this species produce very low roars. In this paper, Frey et al. (2005) investigated the laryngeal anatomy and the roaring vocalizations of the muskox. Roars in both sexes are characterised by a pulsed structure, with a pulse rate of 20 Hz on average. The larynx size of adult male and female are remarkably similar (i.e. almost identical larynx size and vocal cord length). Both sexes possess a potentially inflatable ventrorostral laryngeal ventricle, which could serve to increase the amplitude of roaring or to act as an additional resonance space. The only difference between the sexes is a voluminous fat pad in the medial portions of the vocal cords of adult males, but not of females. However, this pad does not seem to induce important differences between the pitch of males and females. Muskoxen thus differ from other species with similar mating systems (e.g. fallow deer, red deer, elephant seals), in which strong sexual dimorphism is accompanied by distinct acoustic differences.

The two last papers selected for this Virtual Issue on sound production mechanism investigated the link between vocal tract length and formant frequencies in canids (Plotsky et al. 2013) and fallow deer (McElligott et al. 2006), respectively. Plotsky et al. (2013) present one of the first clear evidence that formants provide good, honest vocal cues of signaller size. The authors tested the link between vocal tract length, measured from X-ray images, and measures of body size in Portuguese water dogs (Canis lupus familiaris) and Russian silver foxes (Vulpes vulpes). They show that the oral component of the vocal tract, which determines formant frequencies, is strongly related to body size. McElligott et al. (2006) investigated the link between vocal tract elongation and formant frequencies in fallow deer (Dama dama). This species possesses a mobile larynx that can be retracted during vocalizations. The authors show, using audio and video recordings of mature, groaning fallow bucks, that individuals can increase their vocal tract length on average by 52% during vocalization. The highest formants (3-6), which strongly depend on the vocal tract length, are lowered, while the lowest formants (1-2), which depend more on the shape of the vocal tract, show minimal change during laryngeal retraction. This phenomenon could be used by males to exaggerate their perceived body size.

We hope that you enjoy reading this free collection of papers on various modes of sound production and adaptions published in Journal of Zoology.



Fant, G. (1960). Acoustic theory of speech production. The Hague: Mouton.

Remmers, J.E. and H. Gautier, Neural and Mechanical Mechanisms of Feline Purring. Respiration Physiology, 1972. 16: p. 351-361.

Titze, I.R. (1994). Principles of vocal production. Englewood Cliffs: Prentice-Hall.

New Journal of Zoology Podcast

28 07 2014

A new episode of the Journal of Zoology podcast is now available and you can listen to it here.

Journal of Zoology PodcastIn this episode, Laia Mestre tells us how predators by just their presence are able to affect the behaviour of their prey, such as when spiders change their behaviour when they detect ant cues in their environment. We will also hear from Georgia Cummings about a particular case of bat pollination in New Zealand and how unique such a phenomenon is in a temperate ecosystem, and we learn from Richard Holland what mechanisms and environmental cues migratory birds are using to navigate the globe in so-called ‘true navigation’.

You may subscribe in iTunes to receive the latest Journal of Zoology podcasts.

Elina Rantanen

Recently Published in the Journal

12 06 2014

Urban canyon effect: storm drains enhance call characteristics of the Mientien tree frog

Mientien tree frog calling in the drain (photo by Wen-Hao Tan)

Mientien tree frog calling in the drain (photo by Wen-Hao Tan)

Acoustic signals play fundamental roles in anuran communication by facilitating social interactions, and for many species, successful reproduction depends on long-range propagation and perception of advertisement calls. Several anurans have been shown to exploit habitat features, such as tree holes for their resonance effects, to improve mating call transmission. In an urban environment, such habitat features might also include man-made structures that animals learn to use for acoustic communication. In Taiwan, male Mientien tree frogs Kurixalus idiootocus frequently perch and call in roadside concrete drainages, suggesting that they are using these anthropogenic structures to assist call transmission. The authors of a paper recently published in Journal of Zoology tested this assumption by a combination of field and indoor experiments. Wen-Hao Tan et al. conducted a field survey of whether male Mientien frogs preferred calling inside the storm drains than outside them, and a playback experiment in the field to verify whether the propagation of calls emitted inside drains is enhanced. They also constructed a replica of a concrete drain in the lab to study whether male frogs selected perches inside the drains that facilitated better call transmission.

Field work in action (photo by Y. Kirk Lin)

Field work in action (photo by Y. Kirk Lin)

The field survey indicated that male Mientien tree frogs preferred calling inside rather than outside drains, and the playback experiment showed that calls emitted from inside drains were enhanced in both amplitude and note duration. The lab experiment showed that males preferred a particular type of call perch, although there was no difference in sound properties between random locations inside the drain model and the preferred perch location. Although it still needs to be verified whether the enhanced call transmission of male Mientien frogs calling inside the storm drains also means that they have better mating success, with these ‘urban canyons’, this study shows a novel effect of anthropogenic structures on bioacoustics.

This paper has recently featured in Nature News, Discovery News and several other news sites across the globe.

Elina Rantanen

New Journal of Zoology Podcast

9 04 2014

Journal of Zoology PodcastA new episode of the Journal of Zoology podcast is now available and you can listen to it here.

In this episode, David Hone tells us how the behaviour of extinct animals like dinosaurs can be deduced from the fossil record, we learn from Tomasz Wesolowski about parasites that manipulate the behaviour of their hosts for their own advantage, and Gus Mills talks to us about their new findings on cheetah cub mortality and how they affect conservation planning for cheetahs.

You may subscribe in iTunes to receive the latest Journal of Zoology podcasts.

Elina Rantanen

Hidden Gem

6 03 2014

The Experimental Proof of the Protective Value of Colour and Markings in Insects in reference to their Vertebrate Enemies

This ‘hidden gem’ from 1887 published in the Proceedings of the Zoological Society of London, the predecessor of Journal of Zoology, is an article written by E.B. Poulton about aposematism before he actually introduced the term in his book The Colours of Animals, published in 1890. It is essentially a review article summarising, comparing and discussing the existing data from various experiments testing Alfred Russel Wallace’s original idea of the use of warning colours in prey to put off predators from attacking them.

The article begins with a brief history of the idea, originating from correspondence between Darwin and Wallace. Puzzled by bright, conspicuous colours in caterpillars which could not possibly be explained by sexual selection, Darwin asked Wallace to suggest some other explanation and adaptive value for these bright colours. Wallace proposed that, as Poulton put it, ‘the gaudy colouring acts as an indication of something unpleasant about its possessor’, such as a nauseous taste or smell, and it would thus be to the advantage of the prey to be as conspicuous as possible to warn experienced predators of their foul qualities. Wallace’s idea had subsequently been tested and proven plausible. However, in this paper, Poulton points out that ‘the acquisition of an unpleasant taste or smell, together with a conspicuous appearance, is so simple a mode of protection, and yet ex hypothesi so absolutely complete, that it seems remarkable that more species have not availed themselves of this means of defence. What can be the principle which works in antagonism to such a mode of protection?’ As one explanation, Poulton proposes that this strategy would become less effective the more common it becomes among the prey, as predators might then start eating the foul-tasting prey if they would otherwise starve. It was indeed Poulton who introduced the idea of frequency-dependent selection in his later work, but he was clearly already contemplating this idea when he wrote this article.

This paper acts as a wonderful summary of the development of the theory of aposematism and is teeming with references to Wallace and Darwin as well as other famous names such as Bates and Müller regarding their respective theories on mimicry. It is available for free in our ‘Hidden Gems’ section of the Journal of Zoology website.

Elina Rantanen

Author Spotlight – Matt W. Hayward

27 01 2014

Matt HaywardPrey preferences of the lion (Panthera leo)

Matt W. Hayward & Graham I. H. Kerley, Journal of Zoology, 2006, vol. 267, pp. 309-322

Many years ago I moved to South Africa’s Addo Elephant National Park to conduct a post doc on the reintroduction of lions, leopards and spotted hyaenas there. The regional manager for SAN Parks was concerned that the lions would target valuable buffalo and posed a simple question to me – “What are they going to eat?”  I set about answering that question (and this video presents how I did that). Myself and collaborators at the Nelson Mandela Metropolitan University identified the preferred prey of lions and then extended this work to predict and test their diet at other sites. We then found that there was a tight relationship between the biomass of the preferred prey of lions and the density of lions themselves and there is a negative relationship between lion home range size and preferred prey biomass.  This information has been invaluable to conservation managers as they can now predict the diet, home range and carrying capacity of their large predator guild based on the suite of prey present at a site.

Since then, we have expanded this work to look at the rest of the African large predator guild, Eurasian predators and are now working on the prey preferences of American and Australian predators.  We now hold a database of prey preferences based on over 100,000 kills and we will use this to test various hypotheses relating to optimal foraging theory, mesopredator release and the impacts of invasive predators.  It’s an exciting time, but worth pointing out that this research is based on a plethora of natural history style studies and the demise of natural history makes the kind of meta-analysis that we are conducting very difficult in the future.  The publishing paradigm of only valuing high impact papers is not of particular benefit to practical biodiversity conservation.

Matt W. Hayward

New Journal of Zoology Podcast

17 12 2013

JZO Podcast Autumn 2013A new episode of the Journal of Zoology podcast is now online and you can listen to it here.

In this episode, Sara Helms Cahan talks to us about reproductive division of labour in eusocial species and how it emerged spontaneously in harvester ant queens in their lab experiment, we learn from Rudemar Ernesto Blanco how the ecology of extinct sabretooth predators could be deduced from their living analogue such as the southern short-tailed opossum, and Justin Carroll tells us about their field experiment comparing the effectiveness of two contrasting anti-predator strategies, crypsis and aposematism, using artificial prey.

You may subscribe in iTunes to automatically receive the latest Journal of Zoology podcasts.

By Elina Rantanen


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