Rachel A. Page

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

Receiver perception limits the evolution of increasingly elaborate calls in túngara frogs. 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.

Natural history miscellany : Cues for eavesdroppers: do frog calls indicate prey density and quality?

Predators and parasites that eavesdrop on the mating signals of their prey often preferentially select individuals within a prey/host species that produce specific cues. Mechanisms driving such signal preferences are poorly understood. In the túngara frog Physalaemus pustulosus, conspecific females, frog‐eating bats, and blood‐sucking flies all prefer complex to simple mating calls. In this study we assess the natural signal variation in choruses in the wild and test two hypotheses for why eavesdroppers prefer complex calls: (1) prey quality: complex calls indicate better quality of prey/host, and (2) prey density: complex calls indicate higher prey/host density. Call complexity is not correlated with frog length, mass, or body condition, but it does signal higher abundance of prey/host. Thus, increased effectiveness of attack may have played a role favoring the preference for complex calls in eavesdropping heterospecifics.

Social Transmission of Novel Foraging Behavior in Bats: Frog Calls and Their Referents

The fringe-lipped bat, Trachops cirrhosus, uses prey-emitted acoustic cues (frog calls) to assess prey palatability . Previous experiments show that wild T. cirrhosus brought into the laboratory are flexible in their ability to reverse the associations they form between prey cues and prey quality . Here we asked how this flexibility can be achieved in nature. We quantified the rate at which bats learned to associate the calls of a poisonous toad species with palatable prey by placing bats in three groups: (a) social learning, in which a bat inexperienced with the novel association was allowed to observe an experienced bat; (b) social facilitation, in which two inexperienced bats were presented with the experimental task together; and (c) trial-and-error, in which a single inexperienced bat was presented with the experimental task alone. In the social-learning group, bats rapidly acquired the novel association in an average of 5.3 trials. In the social-facilitation and trial-and-error groups, most bats did not approach the call of the poisonous species after 100 trials. Thus, once acquired, novel associations between prey cue and prey quality could spread rapidly through the bat population by cultural transmission. This is the first case to document predator social learning of an acoustic prey cue.

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.

The effect of signal complexity on localization performance in bats that localize frog calls

The fringe-lipped bat, Trachops cirrhosus, uses frog mating calls to detect and locate its prey. The tungara frog, Physalaemus pustulosus, a preferred prey species of this bat, produces two types of sexual advertise- ment calls, simple and complex, and both female frogs and predatory bats prefer complex calls to simple ones. Complex calls differ from simple ones in that they contain chucks: short, broadband suffixes with distinct onsets and offsets, acoustic properties that should maximize binaural comparisons and facilitate localization. We investigated the hypothesis that frog-eating bats prefer the complex calls of tungara frogs to simple ones because they find complex calls easier to localize. We tested bats under experimental con- ditions that mirror the conditions they encounter in nature: we broadcast tungara frog calls with and with- out background noise and with and without intervening obstacles. We broadcast calls either continuously during the hunting approach or only prior to the bats flight to mimic the conditions under which frogs have detected an approaching bat and ceased calling. Bats showed a trend for better localization perfor- mance of complex calls than of simple ones under all treatment conditions. We found significant differ- ences in localization performance in some but not all levels of localization task complexity. This study is the first to offer evidence that an eavesdropping predator shows better localization performance for a pre- ferred signal variant of its prey.

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.

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.

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.

Sensory-based niche partitioning in a multiple predator–multiple prey community

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator–prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.

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.