Voices of the dead: complex nonlinear vocal signals from the larynx of an ultrasonic frog

Abstract

Most vertebrate species use sound to communicate intra-and inter-specifically. The vocal repertoires of vertebrate groups range widely, with mammals and especially primates having greater repertoires and call complexity than amphibians. It is often assumed that an increase in vocal complexity requires a corresponding increase in the neuromuscular machinery involved in phonation (e.g. Gaunt, 1983;Simpson and Vicario, 1990). According to this view, animals that lack sophisticated mechanisms for motor control of the vocal system are limited to producing relatively simple vocal signals. An alternative means for increasing vocal complexity involves the intrinsic nonlinear dynamics of the oscillators in the larynx or syrinx (Fee et al., 1998). The nonlinear properties of the vocal source enable very small, gradual changes in a control parameter (such as the driving respiratory pressure or rate of airflow across the oscillator) to produce abrupt changes in the vibratory mode, resulting in such nonlinear phenomena as period doubling, biphonation, abrupt frequency jumps and deterministic chaos. The relatively recent application of nonlinear dynamics theory to animal communication has fostered a growing interest in the possible importance of nonlinear phenomena in acoustic communication (Fee et al., 1998;Wilden et al., 1998; BantaLavenex, 1999;Fee, 2002;Fitch et al., 2002).We investigated the inherent nonlinear properties of the larynx of a remarkable frog, Amolops tormotus (Ranidae). Whereas most frogs produce relatively simple calls, the vocalizations of A. tormotus are unusual in several respects. First, males of this small species produce a seemingly endless variety of warbling calls that typically contain both upward and downward frequency modulations (Feng et al., 2002). Second, this frog is unique among those studied in using ultrasound for communication. Many A. tormotus calls extend well into the ultrasonic frequency range (Narins et al., 2004). It has been shown that these frogs can detect and respond to ultrasound (Feng et al., 2006). By extending its vocal communication to Most anurans are highly vocal but their vocalizations are stereotyped and simple with limited repertoire sizes compared with other vocal vertebrates, presumably because of the limited mechanisms for fine vocal motor control. We recently reported that the call of the concaveeared torrent frog (Amolops tormotus Fei) is an exception in its seemingly endless variety, musical warbling quality, extension of call frequency into the ultrasonic range and the prominence of subharmonics, chaos and other nonlinear features. We now show that the major spectral features of its calls, responsible for this frog's vocal diversity, can be generated by forcing pressurized air through the larynx of euthanized males. Laryngeal specializations for ultrasound appear to include very thin portions of the medial vocal ligaments and reverse sexual size dimorphism of the larynx -being smaller in males than in females. The intricate morphology of the vocal cords, which ...

Smooth Operator: Avoidance of Subharmonic Bifurcations through Mechanical Mechanisms Simplifies Song Motor Control in Adult Zebra Finches

“…In voiced sound production by vertebrates, the most common low-dimensional attractors are the fixed point (a constant value), limit cycle (any periodic oscillation, such as pure tones and harmonic stacks), torus (e.g., amplitude modulated sounds), and chaotic attractor (“noisy” sounds) (Wilden et al, 1998; Fitch et al, 2002). The attractors underlying voiced sound leave characteristic signatures in spectrograms and therefore spectrographic evidence has been used to identify phenomena of LDC in the vocalizations of the zebra finch (Fee et al, 1998) and several other bird species (Nowicki and Capranica, 1986; Fletcher, 2000; Baker and Logue, 2003; Beckers and ten Cate, 2006; Zollinger et al, 2008), as well as frogs (Suthers et al, 2006), humans, and other mammals (Fachini et al, 2003; Herzel et al, 1995; Mann et al, 2006; Riede et al, 2000; Svec et al, 1996; Titze et al, 1993; Tokuda et al, 2008; Tyson et al, 2007), and one insect (Benko and Perc, 2007). Although spectrographic representation of sound is indeed helpful in identifying potential candidates, only more detailed analysis, such as close-return (CR) plots and phase-space embedding, allow unambiguous identification (Titze et al, 1993; Herzel et al, 1995; Svec et al, 1996; Fletcher, 2000; Riede et al, 2000; Fachini et al, 2003; Mann et al, 2006; Tyson et al, 2007; Tokuda et al, 2008).…”

Nonlinear acoustic complexity in a fish ‘two-voice’ system

“…We took advantage of the readily accessible toadfish sonic organ, the swim bladder, to test the proposed role of coupled peripheral oscillators in generating chaotic calls [4,7,[12][13][14]. Like other toadfishes, the three-spined toadfish's swim bladder has a single vocal muscle completely attached to each bladder wall; however, unlike any other known fish species, there are two completely separate bladders, each with one muscle [5].…”

“…Across the diversity of vocal vertebrates-from fishes to frogs, songbirds and mammals-analysis of communication signals from these taxonomic groups suggests a strong selection for increased call complexity [2 -7]. Complexity in acoustic signals has traditionally been described by patterns of frequency and/or amplitude modulation, or the sequential combination of harmonic and broadband elements [1,4,7]. However, recent application of chaos theory and nonlinear time-series analysis to animal calls [4,8] has revealed a new metric of acoustic complexity that expands frequency profiles beyond this dichotomous categorization of harmonic and broadband calls in both vertebrate [1,4,7,8] and invertebrate lineages [9][10][11].…”

Habitats matter: the incidence of and response to fear screams in a habitat generalist, the vinous-throated parrotbill Paradoxornis webbianus

“…Furthermore, the observation that parrotbills sometimes showed coordinated mobbing behavior in response to scream call playbacks suggests that screaming may serve to attract conspecifics with the goal of soliciting aid. Nonlinearities observed in the acoustic structure of fear screams may further facilitate the approach response in parrotbills because nonlinearity in vocalizations is common across animal taxa and may be an honest signal of urgency, thereby increasing the response of receivers (Hödl and Gollmann 1986;Wilden et al 1998;Fitch et al 2002;Suthers et al 2006;Blumstein et al 2008;Digby et al 2013). Alternatively, parrotbills may approach the sound source to get information about predators that could be later used to escape from those predators (Conover 1994).…”