Patricia L. Jones

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.

Behavioral evidence for eavesdropping on prey song in two Palearctic sibling bat species

Eavesdropping on prey communication signals has never before been reported for a Palearctic bat species. In this study, we investigated whether lesser and greater mouse-eared bats, Myotis blythii oxygnathus and Myotis myotis, find tettigoniid bushcrickets (Tettigoniidae) by eavesdropping on their mate-attraction song. Tettigoniids are known to be the most important prey item for M. blythii oxygnathus, while carabid beetles and other epigaeic arthropods are the most important prey for its sibling species, M. myotis, in many places in Europe. M. myotis locates walking beetles by listening for their rustling sounds. We compared these two species’ response to four acoustic prey cues: calling song of two tettigoniid species, the rustling sound made by walking carabid beetles, and a control tone. Individuals of both bat species attacked the speaker playing tettigoniid song, which clearly indicates that both species eavesdrop on prey-generated advertisement signals. There were, however, species differences in response. M. blythii oxygnathus exhibited stronger predatory responses to the calling song of two species of tettigoniid than to the beetle rustling sound or the control. M. myotis, in contrast, exhibited stronger predatory responses to the beetle rustling and to one tettigoniid species but not the other tettigoniid or the control. Our study (1) for the first time demonstrates eavesdropping on prey communication signals for Palearctic bats and (2) gives preliminary evidence for sensory niche partitioning between these two sympatric sibling bat species.

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.

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.

The influence of past experience with flower reward quality on social learning in bumblebees

Foraging decisions can be influenced by innate biases, previous individual experience and social information acquired from conspecifics. We examined how these factors interact to affect flower colour preference in the large earth bumblebee, Bombus terrestris dalmatinus. Individual bees with no experience foraging on coloured flowers were first tested for innate colour biases on an unrewarded array of blue and yellow artificial flowers. Depending on treatment, bees then acquired individual experience foraging on a colour (either blue or yellow) associated with high-quality sucrose rewards, or a colour with low-quality sucrose rewards, or they did not acquire any individual experience. Bees were then exposed to the alternative colour associated with conspecific demonstrator bees (social information) or the alternative colour with no social information. Bees that had no individual experience visited flower colours that were associated with conspecific demonstrators (social information) but only significantly if the socially demonstrated colour was one for which bees had an innate bias. When bees had individual experience foraging on a colour with high-quality rewards they continued foraging on that colour, and generally did not visit the socially demonstrated alternative colour, regardless of innate colour bias. Alternatively, when bees had individual experience foraging on colours with low-quality rewards, they made more visits to the socially demonstrated alternative flower colour, but only when the alternative colour was the colour for which they had an innate bias. Bees that had no access to social information continued to forage on low-reward coloured flowers. Thus we show that reward quality of resources with which bees have individual experience affects the use of social information but with an important role of innate biases.

Do frog-eating bats perceptually bind the complex components of frog calls?

The mating calls of male túngara frogs, Physalaemus pustulosus, attract intended (conspecific females) and unintended (eavesdropping predators and parasites) receivers. The calls are complex, having two components: a frequency-modulated “whine” followed by 0–7 harmonic bursts or “chucks”. The whine is necessary and sufficient to elicit phonotaxis from females and the chuck enhances call attractiveness when it follows a whine. Although chucks are never made alone, females perceptually bind the whine and chuck when they are spatially separated. We tested whether an unintended receiver with independent evolution of phonotaxis, the frog-eating bat, Trachops cirrhosus, has converged with frogs in its auditory grouping of the call components. In contrast to frogs, bats approached chucks broadcast alone; when the chuck was spatially separated from the whine the bats preferentially approached the whine, and bats were sensitive to whine–chuck temporal sequence. This contrast suggests that although disparate taxa may be selected to respond to the same signals, different evolutionary histories, selective regimes, and neural and cognitive architectures may result in different weighting and grouping of signal components between generalist predators and conspecific mates.

To Scream or to Listen? Prey Detection and Discrimination in Animal-Eating Bats

All animal-eating bats are echolocators, and the vast majority can capture airborne prey (aerial hawking). The literature suggests that >40 % of these same species also take prey from surfaces (substrate gleaning). Innovations in acoustic recording have revealed bats’ high-frequency vocalizations and showed that hawking bats produce calls of greater intensity than calls produced by gleaning bats. In response to bat echolocation calls, many eared insects initiate evasive action, and some tiger moths produce sounds that deter a bat from completing an aerial attack. Bats abort their hawking attacks as a result of having had their echolocation interfered with by the moths’ sounds, by having had previous experience that taught them moths that make sounds tasted bad, or through some combination of the two. Among gleaning bats, the fringe-lipped bat has been well studied with respect to foraging. This bat uses the sexual advertisement calls of male frogs to localize them. Male frogs that produce calls with more complexity are more attractive to female frogs, but are more easily localized by fringe-lipped bats. It had been argued that gleaning bats are unable to locate perched or otherwise substrate-borne prey using echolocation. This is because background echoes were assumed to mask those reflected from prey. Gleaners were believed, instead, to use prey-generated sounds for detection and localization. It is now known that at least one species of bat is able to resolve echoes reflected from large insect prey from the echoes reflected from the vegetation on which the insect is perched.

Consequences of toxic secondary compounds in nectar for mutualist bees and antagonist butterflies

Attraction of mutualists and defense against antagonists are critical challenges for most organisms and can be especially acute for plants with pollinating and non-pollinating flower visitors. Secondary compounds in flowers have been hypothesized to adaptively mediate attraction of mutualists and defense against antagonists, but this hypothesis has rarely been tested. The tissues of milkweeds (Asclepias spp.) contain toxic cardenolides that have long been studied as chemical defenses against herbivores. Milkweed nectar also contains cardenolides, and we have examined the impact of manipulating cardenolides in nectar on the foraging choices of two flower visitors: generalist bumble bees, Bombus impatiens, which are mutualistic pollinators, and specialist monarch butterflies, Danaus plexippus, which are herbivores as larvae and ineffective pollinators as adults. Although individual bumble bees in single foraging bouts showed no avoidance of cardenolides at the highest natural concentrations reported for milkweeds, a pattern of deterrence did arise when entire colonies were allowed to forage for several days. Monarch butterflies were not deterred by the presence of cardenolides in nectar when foraging from flowers, but laid fewer eggs on plants paired with cardenolide-laced flowers compared to controls. Thus, although deterrence of bumble bees by cardenolides may only occur after extensive foraging, a primary effect of nectar cardenolides appears to be reduction of monarch butterfly oviposition.

Overcoming Sensory Uncertainty: Factors Affecting Foraging Decisions in Frog-Eating Bats

Predators forage in complex environments where they must make fast, high-stakes decisions. Foraging decisions are influenced by biases in sensory perception and cognitive processing, learned and remembered information, and environmental factors such as prey availability. In this chapter, we discuss some of the factors that influence decision-making in a neotropical predatory bat species, the fringe-lipped bat , Trachops cirrhosus. This bat hunts frogs and insects by eavesdropping on prey-produced sounds, but its foraging decisions are also influenced by other sources of information, including echoacoustic and gustatory cues . T. cirrhosus quickly learns novel associations between prey cue and quality, can use social information acquired from conspecifics, and forms long-term memories of prey sounds. Research on perception and cognition in this predatory bat, all conducted with wild or wild-caught and temporarily housed individuals, has made this species one of the most well-understood, non-model systems for predator decision-making. Yet there is still much that remains unknown about how and why these predators make the foraging decisions they do.