Sound source perception in anuran amphibians

Abstract

Sound source perception refers to the auditory system's ability to parse incoming sensory information into coherent representations of distinct sound sources in the environment. Such abilities are no doubt key to successful communication in many taxa, but we know little about their function in animal communication systems. For anuran amphibians (frogs and toads), social and reproductive behaviors depend on a listener's ability to hear and identify sound signals amid high levels of background noise in acoustically cluttered environments. Recent neuroethological studies are revealing how frogs parse these complex acoustic scenes to identify individual calls in noisy breeding choruses. Current evidence highlights some interesting similarities and differences in how the auditory systems of frogs and other vertebrates (most notably birds and mammals) perform auditory scene analysis.

Figure 1

Two components of sound source perception in frogs. The basic auditory problem that frogs encounter in natural social aggregations (depicted in the upper left) is that all of the sound pressure waves produced by individual calling males in a chorus add together to form a single, composite sound pressure waveform. This is a general problem in hearing, and it is a specific biological analogue of the human “cocktail party problem” [2]. It is the composite waveform that impinges on the frog’s body and sets the tympana into motion. In order to make sense of the complex acoustic scenes typical of breeding choruses, a listening frog’s auditory system must decompose this composite waveform to create coherent percepts that correspond to individual calling males as distinct sound sources in the environment (depicted in the lower right). Two challenges emerge from this general problem, one related to auditory masking and the other related to auditory grouping. Behavioral and physiological studies of frogs indicate they may overcome these two challenges by exploiting some of the same features of the acoustic scene that enable humans to understand speech under cocktail-party-like listening conditions. Frogs can experience significant release from auditory masking by exploiting spatial separation between signals and noise and by “listening in the dips” of the natural fluctuations that are present in the level of natural chorus noise. Frogs also appear to integrate simultaneous spectral components and temporally separated sound elements using well-known auditory grouping cues related to commonalities shared by the sound elements produced by a single source.

Figure 2

Release from auditory masking in frogs. In the social environment of a breeding chorus, frogs must often contend with high levels of background noise that potentially masks signals of interest. Recent behavioral studies of female Cope’s gray treefrogs (Hyla chrysoscelis) have used adaptive tracking procedures to investigate release from auditory masking in the presence of chorus-like noise by measuring “signal recognition thresholds” (defined as the lowest signal level that elicits phonotaxis) [23, 29, 56] under various listening conditions. (a) When conspecific calls (signals) and chorus-like noise were separated by 90° around a 2-m-diameter circular test arena, signal recognition thresholds were about 4 dB lower compared to conditions in which the same signals and noise were co-localized [23]. (b) Subjects also experienced about 4 dB of masking release when they listened for pulsed advertisement calls presented in chorus-like noise that slowly fluctuating (e.g., sinusoidally amplitude modulated (SAM) noise; 1.25 Hz) compared to when listening in a non-fluctuating, “flat” noise condition [29]. Together, results from such studies indicate that the frog auditory system can exploit spatial separation between signals and noise and temporal fluctuations in background noise levels in recognizing conspecific calls. (Note: Frogs, speakers, and test arenas not drawn to scale.)

Figure 3

Sequential integration in frogs based on common spatial origin. Frog calls typically comprise multiple sound elements (e.g., notes or pulses) separated in time. For many species, recognizing conspecific calls or selecting high-quality mates requires that receivers perceptually bind temporally separated sound elements into coherent “auditory objects.” Several studies directly or indirectly investigating the role of common spatial origin as an auditory grouping cue indicate that frogs may be fairly permissive of spatial incoherence in recognizing or preferring certain calls. (a) In a field playback experiment, males of the Australian quacking frog (Crinia georgiana) were shown to closely match the number of notes in stimulus calls simulating nearby neighbors [40]. However, males gave calls with similar numbers of response notes to 8-note stimulus calls coming from one direction and composite 8-note calls in which the first and second four notes of the call came from speakers separated by 180° [40]. (b) Laboratory studies of phonotaxis in túngara frogs (Engystomops pustulosus) have also found that females can be permissive of wide angular separations between the preferred “whine” and “chuck” components of complex calls [45]. Whines (w) presented alone elicited robust phonotaxis (indicated here by orientation angles at which females exited the circular test arena relative to the position of the speaker broadcasting the stimulus [45]. Chucks (c) alone failed to elicit phonotaxis; however, whine-chuck sequences elicited phonotaxis directed toward the chuck even when it was separated from the whine by up to 135° [45]. Together, these and other studies [–44] indicate that frogs can be permissive of spatial incoherence and will perceptually group sounds together even though they originate from different locations.

Figure 4

Can frogs fill in the gaps? Studies of auditory induction in frogs have, thus far, failed to uncover convincing evidence that frogs experience a biological analogue of “phonemic restoration” in hearing illusory signal elements (e.g., pulses) that have been replaced by broadband noise. Auditory induction has been investigated in two species of treefrog using two-choice discrimination tests that exploited female preferences for longer signals that contain more pulses [54, 55]. (a) Females of Cope’s gray treefrog (H. chrysoscelis) [55] prefer relatively longer calls composed of continuous trains of pulses. (b) Introducing short gaps into preferred calls by removing pulses can shift female preferences to shorter but nevertheless continuous pulse trains. (c) Filling these gaps with noise can restore the relative attractiveness of the longer signal when compared to equivalent-duration signals with gaps. (d, e) However, there is no evidence that restored attractiveness results because females hear continuous but illusory trains of pulses; if this were the case, we would expect both (d) females to prefer longer, “gap-filled” calls over shorter trains of continuous pulses (which they do not) and (e) gap-filled calls and continuous pulse trains of equivalent duration to be similarly attractive (which they are not).