You talkin’ to me? Interactive playback is a powerful yet underused tool in animal communication research

Over the years, playback experiments have helped further our understanding of the wonderful world of animal communication. They have provided fundamental insights into animal behaviour and the function of communicative signals in numerous taxa. As important as these experiments are, however, there is strong evidence to suggest that the information conveyed in a signal may only have value when presented interactively. By their very nature, signalling exchanges are interactive and therefore, an interactive playback design is a powerful tool for examining the function of such exchanges. While researchers working on frog and songbird vocal interactions have long championed interactive playback, it remains surprisingly underused across other taxa. The interactive playback approach is not limited to studies of acoustic signalling, but can be applied to other sensory modalities, including visual, chemical and electrical communication. Here, I discuss interactive playback as a potent yet underused technique in the field of animal behaviour. I present a concise review of studies that have used interactive playback thus far, describe how it can be applied, and discuss its limitations and challenges. My hope is that this review will result in more scientists applying this innovative technique to their own study subjects, as a means of furthering our understanding of the function of signalling interactions in animal communication systems.     

Eavesdropping and signal matching in visual courtship displays of spiders

Eavesdropping on communication is widespread among animals, e.g. bystanders observing male-male contests, female mate choice copying and predator detection of prey cues. Some animals also exhibit signal matching, e.g. overlapping of competitors' acoustic signals in aggressive interactions. Fewer studies have examined male eavesdropping on conspecific courtship, although males could increase mating success by attending to others' behaviour and displaying whenever courtship is detected. In this study, we show that field-experienced male Schizocosa ocreata wolf spiders exhibit eavesdropping and signal matching when exposed to video playback of courting male conspecifics. Male spiders had longer bouts of interaction with a courting male stimulus, and more bouts of courtship signalling during and after the presence of a male on the video screen. Rates of courtship (leg tapping) displayed by individual focal males were correlated with the rates of the video exemplar to which they were exposed. These findings suggest male wolf spiders might gain information by eavesdropping on conspecific courtship and adjust performance to match that of rivals. This represents a novel finding, as these behaviours have previously been seen primarily among vertebrates.     

Digital video playback and visual communication in lizards

Experimental analyses of dynamic visual signals have to overcome the technical obstacle of reproducing complex motor patterns such as those found in courtship and threat displays. Video playback offers a potential solution to this problem, but it has recently been criticized because of sensory differences between humans and nonhuman animals, which suggest that video stimuli might be perceived as deficient relative to live conspecifics. Quantitative comparisons are therefore necessary to determine whether video sequences reliably evoke natural responses. Male Jacky dragons, Amphibolurus muricatus, compete for territories using complex displays delivered in a rapid stereotyped sequence. We evaluated video playback as a technique for studying this visual signal. Digital video sequences depicting a life-sized displaying male were indistinguishable from live male conspecifics in the rate and structure of aggressive displays evoked. Other measures of social behaviour suggested that video stimuli were more effective in this context. Lizards produced significantly more appeasement displays and had higher rates of substrate licking and locomotor activity in response to video playback than to confined male opponents, which failed to produce aggressive displays. Lizards tracked temporal changes in the display rate of video stimuli and were also sensitive to individual differences in morphology and behaviour between video exemplars. These results show that video stimuli are appropriate for the experimental analysis of Jacky dragon aggressive displays. We compare the potential shortcomings of video playback with those of other techniques and conclude that no approach offers a panacea, but that several have complementary characteristics. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Can video images imitate real stimuli in animal behaviour experiments?

The use of video images in place of natural stimuli in animal behaviour experiments is reviewed. Unlike most other artificial means of stimulus presentation, video stimuli can depict complex moving objects such as other animals, preserving the temporal and spatial patterns of movement precisely as well as colour and sounds for repeated playback. Computer editing can give flexibility and control over all elements of the stimulus. A variety of limitations of video image presentation are also considered. Televisions and video monitors are designed with human vision in mind, and some non-human animals that differ in aspects of visual processing such as their colour vision, critical flicker-fusion threshold, perception of depth and visual acuity, may perceive video images differently to ourselves. The failure of video stimuli to interact with subjects can be a drawback for some studies. For video to be useful, it is important to confirm that the subject animal responds to the image in a comparable way to the real stimulus, and the criteria used to assess this are discussed. Finally, the contribution made by video studies to date in the understanding of animal visual responses is considered, and recommendations as to the future uses of video are made.     

Computer-manipulated stimuli as a research tool in Mozambique tilapia <Emphasis Type="Italic">Oreochromis mossambicus</Emphasis>

Multimodal communication is essential in social interactions in cichlid fish, including conspecifics’ recognition, agonistic interactions and courtship behaviour. Computer-manipulated image stimuli and sound playback offer powerful tools to assess the relative relevance of visual and acoustic stimuli in fish behavioural studies, but these techniques require validation for each taxon. The aim of the present study was to investigate whether Mozambique tilapia Oreochromis mossambicus responds to computer-manipulated visual stimuli and acoustic playback. Six experiments were conducted: computer animation playback, video playback, interaction with a mirror, presentation of a live male in a jar alone and combined with courting sound playback or with white noise playback. Individual agonistic interactions (lateral displays, up and down swimming, butting) and courting behaviours (tilting leading, digging) were tallied for each experiment. Our results suggest that non-interactive computer-manipulated visual stimuli is not a suitable tool in behavioural research with Mozambique tilapia. In contrast, interaction with a live male in a jar seems to remain the best visual research instrument inducing significant strong behavioural responses. Although none or only a few agonistic interactions were observed towards video playbacks or computer animations, such interactions significantly increased towards a male in jar and were modulated by courtship sound playback, suggesting the additional relevance of sound playback as a tool in behavioural research with Mozambique tilapia, including the study of multimodal signalling.     

The deterrent effect of bird song in territory defense

Using the responses of territory owners to playback to inferthe territorial function of acoustic signals is common practice.However, difficulties with interpreting the results of suchexperiments have obscured our understanding of territorial signalling.For instance, a stronger response to playback is often interpretedas more aggressive, but there is no consensus as to whetherthis should be in response to the least or most threateningsimulated intruder. Rather than following a gradual increaseor decrease, the relationship between signal intensity and responsestrength may instead describe a peaked curve. We manipulatedbanded wren (Thryophilus pleurostictus) songs to simulate low-,median-, and high-performance singers and used these songs asstimuli in playback experiments. Banded wrens were less likelyto approach the high-performance stimulus compared with thelow- and median-performance stimuli. However, the birds thatdid approach the high-performance stimulus sang more than thosethat approached the low-performance stimulus. In addition, birdswere more likely to match the songs when exposed to the median-and high-performance stimuli compared with the low-performancestimuli, and song matching predicted approach behavior. Theseresults are in accordance with theoretical models of aggressiveencounters in which low-performance opponents are challengedwithout further assessment. Median- and high-performance opponents,however, may require further assessment, and the latter maybe perceived as too intimidating for approach.     

Song switching and agonistic stimulation in the song sparrow (Melospiza melodia): five tests

Male song sparrows in southeastern Ontario have repertoires of five to 11 distinct song types. The singer repeats each song type a variable number of times before switching to another type. Analysis of territorial singing suggested that rate of switching song types is positively correlated with intensity of agonistic stimulation, where ‘agonistic’ signifies conflict-related. The song-switching hypothesis was tested with playback experiments which varied stimulus intensity in five different ways: (1) presence or absence of song stimuli; (2) addition of visual to auditory stimuli; (3) location of the song stimulus 20 m inside or outside territory; (4) nesting phases of the subjects; and (5) switching rate and rate of novel song type production of the playback (i.e. stimulus versatility). The subjects' switching rates and flight rates consistently increased with greater stimulation, although song rate tended to remain unaffected. The signalling of response intensity through adjustments in switching rate exemplifies how song repertoires function in agonistic communication.     

Plasticity of aggressive signalling and its evolution in male spring peepers, Pseudacris crucifer

Acoustic communication is important for determining and maintaining intermale spacing in breeding aggregations of anurans and insects. Because the number and proximity of signalling males can show extensive temporal and spatial variation, we should expect to find mechanisms that permit males to modify their signalling behaviour in ways that balance the needs to attract females and defend their calling space. We conducted two field playback experiments to investigate the role of plasticity in male aggressive signalling in intermale spacing of spring peepers (Anura, Hylidae). In the first experiment, we found a positive correlation between the amplitude of the advertisement calls of a male's nearest neighbour and the stimulus amplitude at which the male first produced aggressive calls. In the second experiment, repeated presentations of advertisement calls above a male's aggressive threshold resulted in rapid decreases in aggressive signalling and significant, but temporary, elevations of aggressive thresholds. We suggest that short-term habituation to a neighbour's calls could function as a proximate mechanism for plasticity in aggression that would allow males to accommodate nearby callers while also tracking fluctuations in the local density of calling individuals. In a third experiment, we examined female choice as an ultimate-level explanation for plasticity in male aggression. Females preferred advertisement calls to aggressive calls, but this preference was weak and was abolished by a 6-dB reduction in the amplitude of the advertisement call. We suggest that female preferences probably function as only one possible source of selection on plasticity in male aggressive signalling and propose energetic limitations as an additional source of selection. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Responses to song playback vary with the vocal performance of both signal senders and receivers

Mating signals of many animal species are difficult to produce and thus should indicate signaler quality. Growing evidence suggests that receivers modulate their behaviour in response to signals with varying performance levels, although little is known about if and how responses are affected by receiver attributes. To explore this topic we conducted two experiments with swamp sparrows, Melospiza georgiana, in which we challenged territorial males with playback of songs with trill rates that were natural, digitally reduced, or digitally elevated (control-, low- and high-performance stimuli, respectively). In our first experiment, we found that males responded more aggressively to control songs than to low-performance stimuli, that low-performance stimuli with the most severe trill-rate reductions elicited the weakest aggressive responses, and that the subjects'' own trill rates predicted aggressive responses. In our second experiment, we found that male responses to high-performance stimuli varied significantly, in ways predicted by two factors: the degree to which we had elevated stimulus performance levels of high-performance stimuli, and subjects'' own vocal performance levels. Specifically, males were less aggressive towards stimuli for which we had elevated performance levels to higher degrees, and subject males with higher vocal performances themselves responded more aggressively. These findings together offer a novel illustration of how responses to aggressive signals may rely not just on signal attributes, but also on attributes of responding animals themselves.     

Graded Aggressive Calls in the African Painted Reed Frog Hyperolius marmoratus (Hyperoliidae)

The African painted reed frog, Hyperolius marmoratus, has a potentially complex communication system. Advertisement calls and aggressive calls, although distinct from each other, are in fact two ends of a continuum of graded calls. Playback experiments using standard advertisement calls showed that males increased the proportion of aggressive calls as the stimulus intensity was increased. In addition, three characteristics of the aggressive calls changed in response to higher playback levels. Males increased the number of pulses/call, increased call duration, and decreased dominant frequency. Aggressive calling occurred primarily during the early hours of the night, with considerable overlap with times when females were searching for mates in the chorus. Females tested in two-choice arena trials discriminated against aggressive calls in favor of advertisement calls. It is suggested that aggressive calls reduce a male's ability to attract a female and that a graded signalling system may enable males to escalate agonistic encounters with other males without rendering calls completely unattractive to females.     

The Responses of Duetting Antbirds to Stereo Duet Playback Provide Support for the Joint Territory Defence Hypothesis

In multiple animal taxa, including many birds and primates, members of mated pairs produce coordinated acoustic displays known as duets. By observing the behaviour of territorial animals as they respond to playback‐simulated duets of rivals, we can gain insight into the behavioural significance of vocal duets. Playback experiments, however, have been conducted across a very narrow range of duetting animals. Furthermore, many studies have been conducted with single‐speaker playback, whereas stereo‐speaker playback offers more spatially realistic simulation of duets. Moreover, by evaluating the reactions of animals to separate loudspeakers broadcasting male and female duet contributions, we can study the interactions of both males and females with same‐sex vs. opposite‐sex rivals. We used a paired experimental design to broadcast duet stimuli through a single‐speaker and a stereo‐speaker apparatus to 30 pairs of duetting barred antshrikes Thamnophilus doliatus in Costa Rica. Our goals were (1) to evaluate whether territorial antbirds respond more aggressively to male vs. female duet components and (2) to assess aggressive responses of antbirds towards single‐speaker vs. stereo‐speaker playback. Neither males nor females differentiated between the loudspeaker simulating the male vs. female duet contribution during stereo‐speaker playback trials. Barred antshrikes displayed significantly stronger responses to stereo‐speaker playback compared with single‐speaker playback. Males displayed stronger playback responses than females with closer, quicker and more vocal responses. These results provide evidence for a joint resource defence function of antbird duets given that pairs responded together with equivalent intensity to male and female simulated intruders. This is the first study to show that although duetting is an aggressive territorial signal, birds do not necessarily respond to sex‐specific components of duets. Our results support the idea that spatially realistic stereo presentation of duet stimuli is critical for experimental duet research.     

A field test of the audibility of urban versus rural songs in mountain chickadees

Anthropogenic noise can mask avian vocalizations, and several urban‐dwelling species adjust frequency or amplitude of vocalizations in ways that appear to compensate for increased noise levels. Playback studies have investigated whether receivers differentiate between signals produced by rural and urban males, but it is difficult to determine whether differential response to stimulus reflects differences in audibility versus perceived differences in male signals/condition that result from urban settlement. Here, we performed paired‐playback trials to determine whether mountain chickadees (Poecile gambeli) differentiate urban versus rural songs when both stimuli were broadcast within noise. For each playback, stimuli were played in short bouts starting at a low signal‐to‐noise ratio and increasing in relative amplitude with each successive bout. If the primary function of adjusted urban songs is propagation in noise, we hypothesized that focal males would respond sooner to urban versus rural playbacks (detect at lower signal‐to‐noise ratios). If urban songs solely encode information about the male's condition (such as increased aggression), then we predicted only a differential aggressive response to playbacks once detected. If urban songs both increase propagation and embed information on male condition, we predicted a combination of both response types. We found no difference in latency to first response in urban versus rural songs, but some evidence for differential aggression to playback dependent on both stimulus type (urban vs. rural) and local ambient noise levels; focal males in noisy (urban) sites responded aggressively to both stimulus types, whereas focal males in quiet (rural) sites responded more aggressively to urban than to rural stimuli. This context‐dependent discrimination may be the result of increased aggression in urban habitats, improved communication in noisy habitats by urban signallers and receivers, or some combination of the two.     

The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback

Acoustic signals produced by most anurans are accompanied by inflation of a conspicuous vocal sac. We presented female túngara frogs, Physalaemus pustulosus, with acoustic playback of the male advertisement call, synchronized with a video playback of vocal sac inflation. Females significantly preferred a stimulus combination including vocal sac inflation over an identical set of stimuli with the vocal sac inflation removed. Neither a moving rectangle bearing the gross contrast and spatiotemporal properties of the vocal sac inflation sequence, nor the image of a noncalling male significantly enhanced the attractiveness of the acoustic stimulus. Both the form and spatiotemporal properties of the vocal sac thus appear to be salient to females. The results indicate that the vocal sac can serve as a visual cue, which may account for the conspicuous pigmentation found on the vocal sacs of males in many species. Gular inflation in synchrony with a call may function to facilitate female localization of individual males in an aggregation.     

Considerations on the use of video playbacks as visual stimuli: the Lisbon workshop consensus

This paper is the consensus of a workshop that critically evaluated the utility and problems of video playbacks as stimuli in studies of visual behavior. We suggest that video playback is probably suitable for studying motion, shape, texture, size, and brightness. Studying color is problematic because video systems are specifically designed for humans. Any difference in color perception must lead to a different color sensation in most animals. Another potentially problematic limitation of video images is that they lack depth cues derived from stereopsis, accommodation, and motion parallax. Nonetheless, when used appropriately, video playback allows an unprecedented range of questions in visual communication to be addressed. It is important to note that most of the potential limitations of video playback are not unique to this technique but are relevant to all studies of visual signaling in animals. Received: 20 October 1999 / Accepted: 5 November 1999     

An evaluation of video playback using Xiphophorus helleri

Video playback is being increasingly used as a technique for behavioural research. The importance of critically evaluating the effectiveness of video playback is clear, as available video technology is not designed for nonhuman visual systems. We discuss several aspects concerning the perception of video images that could lead to inconclusive or erroneous results. Researchers should verify that behaviour observed in response to video playback is comparable to behaviour observed in response to live animals. We conducted such a verification using live and video playback methods to measure female response to swords of varying lengths in the green swordtail, Xiphophorus helleri. Using both methods, female response appeared to be an increasing function of male sword length. Females did not differ in their response to live and video versions of noncourting, noninteractive males, however, females tended to prefer video playbacks of males with longer swords, a result that has also been found in experiments using live males. These results suggest that females express the same qualitative mating preference, but not necessarily the same quantitative preference, for sword length when viewing video stimuli. Several methodological factors that may contribute to an apparent difference in the strength of the preference are discussed. Despite these differences, both methods produced comparable results; female response to sworded males tended to increase as sword length increased. These experiments demonstrate that video playback is an effective method to measure female preferences accurately in X. helleri and provide an example of how video playback can be evaluated in other species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Memory-dependent adjustment of vocal response latencies in a territorial songbird

Vocal interactions in songbirds can be used as a model system to investigate the interplay of intrinsic singing programmes (e.g. influences from vocal memories) and external variables (e.g. social factors). When characterizing vocal interactions between territorial rivals two aspects are important: (1) the timing of songs in relation to the conspecific’s singing and (2) the use of a song pattern that matches the rival’s song. Responses in both domains can be used to address a territorial rival. This study is the first to investigate the relation of the timing of vocal responses to (1) the vocal memory of a responding subject and (2) the selection of the song pattern that the subject uses as a response. To this end, we conducted interactive playback experiments with adult nightingales (Luscinia megarhynchos) that had been hand-reared and tutored in the laboratory. We analysed the subjects’ vocal response latencies towards broadcast playback stimuli that they either had in their own vocal repertoire (songs shared with playback) or that they had not heard before (unknown songs). Likewise, we compared vocal response latencies between responses that matched the stimulus song and those that did not. Our findings showed that the latency of singing in response to the playback was shorter for shared versus unknown song stimuli when subjects overlapped the playback stimuli with their own song. Moreover birds tended to overlap faster when vocally matching the stimulus song rather than when replying with a non-matching song type. We conclude that memory of song patterns influenced response latencies and discuss possible mechanisms.     

Functions of duetting in the tropical boubou, Laniarius aethiopicus: territorial defence and mutual mate guarding

Duetting, found in many animal taxa, is still a poorly understood form of signalling behaviour despite numerous hypotheses to explain its function. One contentious issue is whether duetting is a cooperative endeavour or signals conflict between the sexes. We studied the function of duetting in the tropical boubou, using interactive playback experiments. We staged encounters by presenting paired birds with four variants of each of four duet types (neighbour and stranger solos and neighbour and stranger duets). Multiple lines of evidence suggest that both joint territorial defence and mutual mate guarding are important functions of duetting, and that both cooperation and conflict between males and females have shaped duetting behaviour. Of a repertoire of 12 duet types, eight were used for joint territorial defence. Two of these eight duet types were probably also used for mutual mate guarding, suggesting that individual duets can have multiple functions. We found an unusual response for duetting birds in that females often synchronized notes with male solo playback to form precise duets. In turn, males attempted to jam the song of rivals when females joined the song of male solo playback, providing further evidence for the importance of acoustic mate guarding. Song jamming by males has not previously been described for duetting species. Finally, we suggest that the repertoire of duet types is used to fine-tune territorial encounters in a network environment of multiple interactants.     

Interaction effects of corticosterone and experience on aggressive behavior in the green anole lizard

Aggressive encounters are accompanied by a release of stress hormone, and this corticosterone (CORT) secretion could influence aggressive behavior in subsequent encounters. We investigated the modulating effects of CORT on aggressive behavior in the context of a 5-day social experience in male green anole lizards. In Experiment 1, we measured plasma CORT levels in animals that were exposed for different times to aggressive males. In Experiment 2, using metyrapone, a CORT synthesis blocker, we tested whether CORT secretion in response to the aggressive stimulus plays a role in experience-dependent facilitation of aggressive behavior. We hypothesized that aggressive encounters would increase plasma CORT levels, and that blocking CORT synthesis with metyrapone treatment during the aggressive encounter would cause an animal to become more aggressive. We also tested whether blocking CORT would interfere with the influence of 5-day social experience on animals' behavior in a subsequent aggressive encounter. Animals that were exposed to another male showed higher plasma CORT levels immediately after the 10 min encounter than animals exposed to the non-social video, and this high level was maintained through day 5. Within the aggressive video groups, in Experiment 2, there was a distinctly different pattern in displays depending on drug condition: vehicle-injected animals showed gradual increases followed by decreases in aggressive behavioral responses to the video as the five days proceeded (habituation), while animals injected with metyrapone started out with high aggressive behavior and did not decrease behavioral responses at later trials (no habituation). Finally, when tested with a novel conspecific on day 6, animals previously injected with metyrapone showed no higher aggression than did animals previously injected with vehicle and exposed to the aggressive video. These results suggest that blocking CORT synthesis during the exposure to the aggressive video induced animals to remain aggressive toward the repetitive stimulus without habituating, while not becoming more aggressive than controls toward a novel challenger.     

Latent song type memories are accessible through auditory stimulation in a hand-reared songbird

The production of learned vocalizations such as in birdsong is often used to judge whether stimuli had been memorized upon their presentation. However, failures in the imitation of certain song patterns may also reflect impaired development of motor programmes or impaired memory retrieval rather than failures in stimulus memorization during auditory acquisition. To study this issue, we confronted adult hand-reared nightingales, Luscinia megarhynchos, with interactive playback experiments and used vocal matching as a behavioural tool to investigate their song type memories. Vocal matching is a common pattern-specific response that songbirds use in territorial countersinging. We distinguished two forms of pattern-specific matching: (1) song type matching (i.e. a bird replied with the same song type as the stimulus song), and (2) song group matching (i.e. the bird replied with a different song type which was, however, sequentially associated with the playback song presented earlier, i.e. during the tutoring). Some subjects used both song type and song group matching in response to song types they had not imitated from the tutor programme prior to the playback experiments. Our results indicate that nightingales store more song types in their sensory phase than they spontaneously recall from memory as adults. That is, memories of song types that were not performed in overt behaviour could be activated by vocal interactions, here induced by the interactive playback. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Response to Video and Computer-animated Images by the Tiger Barb, Puntius tetrazona

Video playback has become an important tool for testing certain questions about animal visual perception. While a few studies have compared the response of test subjects to live and video stimuli, it is generally assumed a priori that the animals will respond to the video image as if it were real. Since video devices are tuned to the spectral sensitivities and flicker fusion frequencies of the human eye and brain, it is important to conduct preliminary tests to compare the response of test subjects between live and video images. Here we compare schooling behavior of tiger barbs, Puntius tetrazona, when presented with a school of live fish, an analog video school of fish and a video of a computer-animated school of fish. Test subjects did not show a significantly different schooling behavior response to any of these stimuli. Additionally, when given the choice of schooling with a conspecific versus a heterospecific, tiger barbs schooled significantly more often with the conspecifics for all three stimulus formats. This study provides evidence that tiger barbs do not choose to discriminate between live and video models of fish and that this technique can be used to test future questions concerning visual perception for this species.