Signal Perception in Frogs and Bats and the Evolution of Mating Signals

Abstract

Psychophysics measures the relationship between a stimulus's physical magnitude and its perceived magnitude. Because decisions are based on perception of stimuli, this relationship is critical to understanding decision-making. We tested whether psychophysical laws explain how female túngara frogs (Physalaemus pustulosus) and frog-eating bats (Trachops cirrhosus) compare male frog calls, and how this imposes selection on call evolution. Although both frogs and bats prefer more elaborate calls, they are less selective as call elaboration increases, because preference is based on stimulus ratios. Thus, as call elaboration increases, both relative attractiveness and relative predation risk decrease because of how receivers perceive and compare stimuli. Our data show that female cognition can limit the evolution of sexual signal elaboration.

Perceptual bias does not explain preference for prey call adornment in the frog-eating bat

“…We used complex calls with chucks as our reference complex call because the number of chucks is known to influence call preference in T. cirrhosus (Akre et al 2011) and because a complex call with three chucks is the stimulus that was used in the original phonotaxis experiment that revealed the preference of T. cirrhosus for complex calls . We modified simple calls to give them one of the six acoustic properties of complex calls (Table 1), creating simple calls that were acoustically "matched" to a complex call for one specific acoustic parameter only.…”

“…For example, within a given species of field cricket, parasitoid Ormia flies prefer individuals that produce songs with longer and more numerous chirps (Wagner 1995). Likewise, predatory bats and parasitic flies eavesdropping on male túngara frogs both prefer adorned to unadorned calls, as do female túngara frogs Bernal et al 2006;Akre et al 2011). As in female mate choice, eavesdropper preferences could originate both from prey/host selection behavior (i.e., optimal foraging; Stephens and Krebs 1986) and from perceptual biases.…”

“…In contrast, eavesdropper preferences based on perceptual biases arise when a prey species evolves a signal that better stimulates the sensory or cognitive systems of the eavesdropper. The tuning of receptor neurons, the anatomy of feature extraction circuits, and general cognitive processes such as Weber's Law all determine the perceptual space experienced by an animal (Akre et al 2011;Ryan and Cummings 2013). If prey produces signals that vary in the parameters that determine the perceptual space of a predator, then some prey signals could be more salient to and therefore preferred by that predator, even when eavesdropping on all signal variants provide similar fitness benefits.…”

“…Male túngaras produce complex calls in the presence of competing males, and complex calls with more than two or three chucks are very rarely produced (Ryan 1985;Bernal et al 2007). Both female frogs (Rand and Ryan 1981) and frog-eating bats Akre et al 2011) prefer (show stronger phonotaxis toward) complex calls over simple calls. For female túngara frogs, this preference has been originally explained by sensory exploitation mechanisms, whereby the adornment of simple calls (adding chucks to the whine) exploits a pre-existing perceptual bias in the female túngara auditory system that pre-dates the evolution of the chuck (Ryan et al 1990; however, see Ron 2008 for an analysis that contradicts this hypothesis).…”

Multimodal cues improve prey localization under complex environmental conditions

“…The male tú ngara frog can produce two types of calls: a simple call, consisting of a downward frequency sweep known as whine, or a complex call, consisting of a whine with one to seven amplitude-modulated pulses, or chucks, added to it [30]. Bats are better at locating the source of a complex caller and when given a choice prefer to attack speakers broadcasting complex calls to speakers broadcasting simple calls [31,32]. The male tú ngara frog also displays a large vocal sac that inflates with the call onset and deflates with call offset [33][34][35].…”