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

Abstract

Acoustic signals play essential roles in social communication and show a strong selection for novel morphologies leading to increased call complexity in many taxa. Among vertebrates, repeated innovations in the larynges of frogs and mammals and the syrinx of songbirds have enhanced the spectro-temporal content, and hence the diversity of vocalizations. This acoustic diversification includes nonlinear characteristics that expand frequency profiles beyond the traditional categorization of harmonic and broadband calls. Fishes have remained a notable exception to evidence for such acoustic innovations among vertebrates, despite their being the largest group of living vertebrates that also exhibit widespread evolution of sound production. Here, we combine rigorous acoustic and mathematical analyses with experimental silencing of the vocal motor system to show how a novel swim bladder mechanism in a toadfish enables it to generate calls exhibiting nonlinearities like those found among frogs, birds and mammals, including primates. By showing that fishes have evolved nonlinear acoustic signalling like all other major lineages of vocal vertebrates, these results suggest strong selection pressure favouring this mechanism to enrich the spectro-temporal content and complexity of vocal signals.

Novel underwater soundscape: acoustic repertoire of plainfin midshipman fish

“…Third, building upon recent reports of the Lusitanian toadfish, Halobatrachus didactylus (Amorim, 2006;Vasconcelos et al, 2012), the three-spined toadfish, Batrachomoeus trispinosus (Rice and Bass, 2009;Rice et al, 2011), and two toadfish species from Belize, Sanopus astrifer and Batrachoides gilbert (see Mosharo and Lobel, 2012), the current study begins to reveal the breadth of intraspecific and interspecific diversity in the spectro-temporal properties of toadfish calls beyond that of species within the genus Opsanus that have predominated the literature for nearly six decades (see below). Fourth, together with our earlier studies of the three-spined toadfish (Rice and Bass, 2009;Rice et al, 2011), we looked in detail at the structure of individual sounds themselves. This includes an in-depth analysis of growls, the least studied but acoustically most variable in structure of midshipman sounds and perhaps toadfish sounds in general (see further discussion in the following section).…”

“…Sample recordings from this same site have appeared in a qualitative context elsewhere Bass and Clark, 2003;Bodnar and Bass, 1997;Lee, 1996;Rice and Bass, 2009;Rice et al, 2011). The inhabitants of each nest were weighed and measured (standard length), and identified as type I male, type II male or female on the basis of size and coloration (see Bass, 1996;Brantley and Bass, 1994).…”

Vocal production complexity correlates with neural instructions in the oyster toadfish (Opsanus tau)

“…1) (Edds-Walton et al, 2002). In chaotic nonlinear signals, the phase-space plot has a distinctive threedimensional, aperiodic structure, whereas linear signals are periodic and often two-dimensional (Elemans et al, 2010;Fitch et al, 2002;Rice et al, 2011). In phase-space, 10 overlaid calls of one male show a distinctive three-dimensional aperiodic attractor (BW1 in Fig.…”

“…Midshipman fish, however, do not exhibit a P1 in their calls (Rice et al, 2011). Of all batrachoidids, the motor control networks in midshipman fish are the best known and considered conserved amongst the batrachoidids as well as vocal tetrapods (Bass et al, 2008).…”

“…The activity of these neural circuits drives an often highly nonlinear vocal system, capable of generating acoustic signals ranging from whistles to complex, irregular vocalisations that exhibit low-dimensional chaos (Elemans et al, 2010;Fitch et al, 2002). Such complex sounds have been reported in fish (Rice et al, 2011), frogs (Suthers et al, 2006), birds (Fletcher, 2000;Zollinger et al, 2008) and various mammals (Fitch et al, 2002). The biomechanics of a peripheral system can impose constraints on its neural control, but also provide opportunities for the emergence of complexity in expressed behaviours (Chiel and Beer, 1997).…”