Ryan C. Taylor

Multimodal signal variation in space and time: how important is matching a signal with its signaler?

SUMMARY Multimodal signals (acoustic+visual) are known to be used by many anuran amphibians during courtship displays. The relative degree to which each signal component influences female mate choice, however, remains poorly understood. In this study we used a robotic frog with an inflating vocal sac and acoustic playbacks to document responses of female túngara frogs to unimodal signal components (acoustic and visual). We then tested female responses to a synchronous multimodal signal. Finally, we tested the influence of spatial and temporal variation between signal components for female attraction. Females failed to approach the isolated visual cue of the robotic frog and they showed a significant preference for the call over the spatially separate robotic frog. When presented with a call that was temporally synchronous with the vocal sac inflation of the robotic frog, females did not show a significant preference for this over the call alone; when presented with a call that was temporally asynchronous with vocal sac inflation of the robotic frog, females discriminated strongly against the asynchronous multimodal signal in favor of the call alone. Our data suggest that although the visual cue is neither necessary nor sufficient for attraction, it can strongly modulate mate choice if females perceive a temporal disjunction relative to the primary acoustic signal.

Risky Ripples Allow Bats and Frogs to Eavesdrop on a Multisensory Sexual Display

Animal displays are often perceived by intended and unintended receivers in more than one sensory system. In addition, cues that are an incidental consequence of signal production can also be perceived by different receivers, even when the receivers use different sensory systems to perceive them. Here we show that the vocal responses of male túngara frogs (Physalaemus pustulosus) increase twofold when call-induced water ripples are added to the acoustic component of a rival’s call. Hunting bats (Trachops cirrhosus) can echolocate this signal by-product and prefer to attack model frogs when ripples are added to the acoustic component of the call. This study illustrates how the perception of a signal by-product by intended and unintended receivers through different sensory systems generates both costs and benefits for the signaler. Calling frogs incidentally produce water ripples that are targeted by rival males and frog-eating bats. Its Complicated Animals have evolved impressive displays used in mate selection. Although intended for the opposite sex of the same species, the potential for eavesdropping is significant. In cases where the sensory signature is the sexual signal itself (such as a bird call), selection from harmful eavesdroppers could result in a reduction in signal intensity that represents a balance between the cost and benefit of the signal. Halfwerk et al. (p. 413), however, show that the physical by-product of a signal can also act as a cue to both intended and eavesdropping recipients. Ripples in the water made by throat sac expansion in calling túngara frogs signal their presence both to rivals and to predatory bats. This physical signature of the call itself cannot be modified; thus, it represents a cost-benefit ratio to calling that cannot be shifted through selection pressure from either side. Thus, physical by-products of sensory signaling create significant complexity in the evolution of sexual signaling.

Interactions of multisensory components perceptually rescue túngara frog mating signals.

Romancing the Frog In túngara frogs, auditory and visual components of mate calling do not naturally occur together. Taylor and Ryan (p. 273, published online 6 June) now show that two signals that are unattractive to female frogs when presented alone become highly attractive when presented together. In a kind of “perceptual rescue,” the unique combination of two signals increased the receivers interest in the previously uninteresting signals. Mating signals that females find unattractive when presented singly become attractive when combined. Sexual signals are often complex and perceived by multiple senses. How animals integrate signal components across sensory modalities can influence signal evolution. Here we show that two relatively unattractive signals that are perceived acoustically and visually can be combined in a pattern to form a signal that is attractive to female túngara frogs. Such unanticipated perceptual effects suggest that the evolution of complex signals can occur by alteration of the relationships among already-existing traits.

Robots in the service of animal behavior.

As reading fiction can challenge us to better understand fact, using fake animals can sometimes serve as our best solution to understanding the behavior of real animals. The use of dummies, doppelgangers, fakes, and physical models have served to elicit behaviors in animal experiments since the early history of behavior studies, and, more recently, robotic animals have been employed by researchers to further coax behaviors from their study subjects. Here, we review the use of robots in the service of animal behavior, and describe in detail the production and use of one type of robot – “faux” frogs – to test female responses to multisensory courtship signals. The túngara frog (Physalaemus pustulosus) has been a study subject for investigating multimodal signaling, and we discuss the benefits and drawbacks of using the faux frogs we have designed, with the larger aim of inspiring other scientists to consider the appropriate application of physical models and robots in their research.

Bats perceptually weight prey cues across sensory systems when hunting in noise

Anthropogenic noise can interfere with environmental information processing and thereby reduce survival and reproduction. Receivers of signals and cues in particular depend on perceptual strategies to adjust to noisy conditions. We found that predators that hunt using prey sounds can reduce the negative impact of noise by making use of prey cues conveyed through additional sensory systems. In the presence of masking noise, but not in its absence, frog-eating bats preferred and were faster in attacking a robotic frog emitting multiple sensory cues. The behavioral changes induced by masking noise were accompanied by an increase in active localization through echolocation. Our findings help to reveal how animals can adapt to anthropogenic noise and have implications for the role of sensory ecology in driving species interactions.

Crossmodal Comparisons of Signal Components Allow for Relative-Distance Assessment

Animals have multiple senses through which they detect their surroundings and often integrate sensory information across different modalities to generate perceptions. Animal communication, likewise, often consists of signals containing stimuli processed by different senses. Stimuli with different physical forms (i.e., from different sensory modalities) travel at different speeds. As a consequence, multimodal stimuli simultaneously emitted at a source can arrive at a receiver at different times. Such differences in arrival time can provide unique information about the distance to the source. Male túngara frogs (Physalaemus pustulosus) call from ponds to attract females and to repel males. Production of the sound incidentally creates ripples on the water surface, providing a multimodal cue. We tested whether male frogs attend to distance-dependent cues created by a calling rival and whether their response depends on crossmodal comparisons. In a first experiment, we showed distance-dependent changes in vocal behavior: males responded more strongly with decreasing distance to a mimicked rival. In a second experiment, we showed that males can discriminate between relatively near and far rivals by using a combination of unimodal cues, specifically amplitude changes of sound and water waves, as well as crossmodal differences in arrival time. Our data reveal that animals can compare the arrival time of simultaneously emitted multimodal cues to obtain information on relative distance to a source. We speculate that communicative benefits from crossmodal comparison may have been an important driver of the evolution of elaborate multimodal displays.

Risks of multimodal signaling: bat predators attend to dynamic motion in frog sexual displays

Many sexual displays contain multiple components that are received through a variety of sensory modalities. Primary and secondary signal components can interact to induce novel receiver responses and become targets of sexual selection as complex signals. However, predators can also use these complex signals for prey assessment, which may limit the evolution of elaborate sexual signals. We tested whether a multimodal sexual display of the male túngara frog (Physalaemus pustulosus) increases predation risk from the fringe-lipped bat (Trachops cirrhosus) when compared with a unimodal display. We gave bats a choice to attack one of two frog models: a model with a vocal sac moving in synchrony with a mating call (multisensory cue), or a control model with the call but no vocal sac movement (unimodal cue). Bats preferred to attack the model associated with the multimodal display. Furthermore, we determined that bats perceive the vocal sac using echolocation rather than visual cues. Our data illustrate the costs associated with multimodal signaling and that sexual and natural selection pressures on the same trait are not always mediated through the same sensory modalities. These data are important when considering the role of environmental fluctuations on signal evolution as different sensory modalities will be differentially affected.

Multimodal cues improve prey localization under complex environmental conditions

Predators often eavesdrop on sexual displays of their prey. These displays can provide multimodal cues that aid predators, but the benefits in attending to them should depend on the environmental sensory conditions under which they forage. We assessed whether bats hunting for frogs use multimodal cues to locate their prey and whether their use varies with ambient conditions. We used a robotic set-up mimicking the sexual display of a male túngara frog (Physalaemus pustulosus) to test prey assessment by fringe-lipped bats (Trachops cirrhosus). These predatory bats primarily use sound of the frogs call to find their prey, but the bats also use echolocation cues returning from the frogs dynamically moving vocal sac. In the first experiment, we show that multimodal cues affect attack behaviour: bats made narrower flank attack angles on multimodal trials compared with unimodal trials during which they could only rely on the sound of the frog. In the second experiment, we explored the bats use of prey cues in an acoustically more complex environment. Túngara frogs often form mixed-species choruses with other frogs, including the hourglass frog (Dendropsophus ebraccatus). Using a multi-speaker set-up, we tested bat approaches and attacks on the robofrog under three different levels of acoustic complexity: no calling D. ebraccatus males, two calling D. ebraccatus males and five D. ebraccatus males. We found that bats are more directional in their approach to the robofrog when more D. ebraccatus males were calling. Thus, bats seemed to benefit more from multimodal cues when confronted with increased levels of acoustic complexity in their foraging environments. Our data have important consequences for our understanding of the evolution of multimodal sexual displays as they reveal how environmental conditions can alter the natural selection pressures acting on them.

Mate Searching Animals as Model Systems for Understanding Perceptual Grouping

A critical component of communication in humans and nonhuman animals is the ability to group signals so that they can be assigned to their correct sources. This is especially true for mate choice behavior, as incorrect stimulus grouping could lead to inaccurate evaluation of signalers by receivers, ultimately resulting in costly mate choice decisions . Sexual signals are often complex, consisting of components that vary in several physical parameters and across sensory modalities. Thus, the mate choice behavior of receivers is well suited for psychophysical tests of the limits and mechanisms of perceptual grouping both within and across sensory modalities. This chapter examines perceptual grouping in comparative models of mate choice behavior. We focus primarily on mate attraction in frogs, reviewing first the effects of spectral, temporal, and spatial parameters on sequential and simultaneous auditory grouping. We then review research on cross-modal perceptual grouping of frog visual and acoustic signals, a perceptual ability analogous to that of grouping human speech with its coincident mouth movements. In addition, we suggest that data from comparative models are not only useful for understanding signal processing in animal communication but also for potentially understanding the fundamental mechanisms receivers use to sort complex signals across all taxa and how such mechanisms may evolve.

Multimodal signaling improves mating success in the green tree frog (Hyla cinerea), but may not help small males

Many anuran amphibians are challenged with the detection of courtship signals in noisy chorus environments. Anurans and other animals partially solve this discrimination challenge by employing auditory mechanisms such as grouping sounds by frequency, time, or spatial location. Animals are also known to employ visual cues as a mechanism of improving auditory signal detection. In this study, we examined the effect of acoustic and visual stimuli on female mate choice preferences in the green tree frog, Hyla cinerea. We used a series of two choice playback tests and added a robotic frog, with an inflatable vocal sac, to test interactions among visual and acoustic signal components. Females preferred vocalizations with faster call rates (i.e., high energy cost) and lower call frequencies (i.e., larger males). When call properties were held equal, females discriminated against an acoustic only stimulus in favor of the combined acoustic/visual multimodal signal. A visual component did not, however, increase the attractiveness of an otherwise unattractive (high-frequency) acoustic signal. Thus, female green tree frogs integrate the visual display into the acoustic communication system and males that are visually accessible can increase their probability of mating success. Visual accessibility, however, is unlikely to improve mating success for small males (high-frequency callers).Significance statementAnimal communication signals are often complex and communicated in multiple sensory channels (e.g., auditory + visual). Female choice is known to be an important mechanism driving signal evolution. Thus, for complex mating signals, a first step in understanding their evolution is to test how females respond to various combinations of components. Here, we tested female mate choice in the green tree frog, H. cinerea, using a combination of audio playbacks and a robotic frog as the visual component. When the audio signal was standardized, females preferred a signal enhanced by a robotic frog. The robotic frog did not increase female responses to an unattractive call (indicative of a small male), however. These results suggest that visual accessibility can improve a male’s chance of mating, but this advantage is context dependent and does not extend to smaller males.