By‐product information can stabilize the reliability of communication

Although communication underpins many biological processes, its function and basic definition remain contentious. In particular, researchers have debated whether information should be an integral part of a definition of communication and how it remains reliable. So far the handicap principle, assuming signal costs to stabilize reliable communication, has been the predominant paradigm in the study of animal communication. The role of by‐product information produced by mechanisms other than the communicative interaction has been neglected in the debate on signal reliability. We argue that by‐product information is common and that it provides the starting point for ritualization as the process of the evolution of communication. Second, by‐product information remains unchanged during ritualization and enforces reliable communication by restricting the options for manipulation and cheating. Third, this perspective changes the focus of research on communication from studying signal costs to studying the costs of cheating. It can thus explain the reliability of signalling in many communication systems that do not rely on handicaps. We emphasize that communication can often be informative but that the evolution of communication does not cause the evolution of information because by‐product information often predates and stimulates the evolution of communication. Communication is thus a consequence but not a cause of reliability. Communication is the interplay of inadvertent, informative traits and evolved traits that increase the stimulation and perception of perceivers. Viewing communication as a complex of inadvertent and derived traits facilitates understanding of the selective pressures shaping communication and those shaping information and its reliability. This viewpoint further contributes to resolving the current controversy on the role of information in communication.     

Defining biological communication

Communication is ubiquitous in biology, and agreement on terms essential for scientific progress. Yet there is no agreed definition of biological communication. Definitions couched in terms of adaptation are often used, but there is significant variability in exactly which criteria are invoked. An alternative is to define communication in terms of information transfer. This article reviews the merits of these approaches, and argues that the former is to be preferred, so long as we demand that both the signal and the response be adaptive, rather than just one or the other, as is common. Specific concerns with the definition are addressed, and it is then explained why an account of communication predicated on information transfer is necessarily derivative upon such an approach. Other alternatives and some variants of the adaptationist definition are also briefly discussed.     

Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wright's (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.     

Heterogeneous tempo and mode of evolutionary diversification of compounds in lizard chemical signals

Important part of the multivariate selection shaping social and interspecific interactions among and within animal species emerges from communication. Therefore, understanding the diversification of signals for animal communication is a central endeavor in evolutionary biology. Over the last decade, the rapid development of phylogenetic approaches has promoted a stream of studies investigating evolution of communication signals. However, comparative research has primarily focused on visual and acoustic signals, while the evolution of chemical signals remains largely unstudied. An increasing interest in understanding the evolution of chemical communication has been inspired by the realization that chemical signals underlie some of the major interaction channels in a wide range of organisms. In lizards, in particular, chemosignals play paramount roles in female choice and male–male competition, and during community assembly and speciation. Here, using phylogenetic macro‐evolutionary modeling, we show for the very first time that multiple compounds of scents for communication in lizards have diversified following highly different evolutionary speeds and trajectories. Our results suggest that cholesterol, α‐tocopherol, and cholesta‐5,7‐dien‐3‐ol have been subject to stabilizing selection (Ornstein–Uhlenbeck model), whereas the remaining compounds are better described by Brownian motion modes of evolution. Additionally, the diversification of the individual compounds has accumulated substantial relative disparity over time. Thus, our study reveals that the chemical components of lizard chemosignals have proliferated across different species following compound‐specific directions.     

Ready to Fight: Reliable Predictors of Attack in a Cooperatively Breeding,Non‐Passerine Bird

Signal reliability is a major focus of animal communication research. Aggressive signals are ideal for measuring signal reliability because the signal referent – attack or no attack – can be measured unambiguously. Signals of aggressive intent occur at elevated rates in aggressive contexts, predict subsequent aggression by the signaler, and elicit appropriate responses from receivers. We tested the ‘predictive criterion’ in smooth‐billed anis, Crotophaga ani, by broadcasting one of two playback types (‘ahnee’ calls only or ‘ahnee + hoot’ calls), presenting a taxidermic mount, and observing the animals’ behavior. Based on the hypotheses that ‘hoot’ calls and ‘throat‐inflation’ displays signal aggressive intent, we predicted that they would be associated with attack, and that signaling rate would increase over the time period leading up to an attack. Indeed, both hoots and throat‐inflation displays reliably predicted attack. The second prediction, that signaling rate increases in the time leading up to attack, was strongly supported for throat‐inflation displays, which increased over the pre‐attack period in both treatments. Hoots increased over the pre‐attack period in ahnee playbacks but not in ahnee + hoot playbacks. Hierarchical signaling systems are characterized by early, less‐reliable predictors of attack, and later, more reliable predictors of attack. During both natural and simulated interactions, the more‐reliable throat‐inflation display tended to precede the less‐reliable hoot call, suggesting that this signaling system is not hierarchical. In a comparison of 11 putative signals of aggressive intent in birds, the throat‐inflation display had the second highest mutual information (reduction in uncertainty) among visual signals and non‐passerine signals while hoots had below‐average mutual information. Natural observations indicate that both hoots and throat‐inflation displays occur in the context of aggressive between‐group encounters, and hoots also occur during within‐group interactions. Throat‐inflation displays appear to be reliable indicators of aggressive intent, but the function of hoot calls is less clear.     

Molecular diagnostics reveal spiders that exploit prey vibrational signals used in sexual communication

Vibrational signalling is a widespread form of animal communication and, in the form of sexual communication, has been generally regarded as inherently short‐range and a private communication channel, free from eavesdropping by generalist predators. A combination of fieldwork and laboratory experiments was used to test the hypothesis that predators can intercept and exploit such signals. First, we developed and characterized PCR primers specific for leafhoppers of the genus Aphrodes and specifically for the species Aphrodes makarovi. Spiders were collected from sites where leafhoppers were present and screened with these primers to establish which spider species were significant predators of this species during the mating period of these leafhoppers. Analysis using PCR of the gut contents of tangle‐web spiders, Enoplognatha ovata (Theridiidae), showed that they consume leafhoppers in the field at a greater rate when signalling adults were present than when nymphs were dominant, suggesting that the spiders were using these vibrations signals to find their prey. Playback and microcosm experiments then showed that E. ovata can use the vibrational signals of male leafhoppers as a cue during foraging and, as a result, killed significantly more male than female A. makarovi. Our results show, for the first time, that arthropod predators can exploit prey vibrational communication to obtain information about prey availability and use this information to locate and capture prey. This may be a widespread mechanism for prey location, one that is likely to be a major unrecognized driver of evolution in both predators and prey.     

穴居啮齿动物震动信号的意义及研究展望

穴居啮齿动物一般生活在黑暗、复杂的地下洞道环境中。营地下生活的特殊栖息环境使其进化出了与环境相适应的震动通讯,用来实现个体或社群间的信息联系。震动通讯是动物界中一种独特的信息传递方式,穴居啮齿动物的震动通讯已成为行为生态学研究的热点之一。了解震动信号发生和接收的部位、特征及其生物学意义,对于完善和发展穴居啮齿动物基础研究具有重大意义。但是,对于穴居啮齿动物来说,其独特的地下栖息生活方式增加了解读震动信号的难度。这些挑战导致穴居啮齿动物震动通讯方面研究进展缓慢、科研文章较少。本文在查阅国内外穴居啮齿动物震动通讯研究文献的基础上,分别从具有震动通讯特征的穴居啮齿动物种类、分布,震动信号发生和接收部位,震动信号的作用以及研究方法等方面进行了概述,并展望了震动信号在鼠害防控、医疗等领域应用的可能性。本文旨在为今后研究穴居啮齿动物震动通讯提供参考。     

Managing predators: The influence of kangaroo rat antipredator displays on sidewinder rattlesnake hunting behavior

Upon sensing predators in their vicinity, many prey species perform antipredator displays that are thought to provide information to the predator that deters it from attacking (predator‐deterrent signals). These displays can be complex, incorporating a variety of signaling elements as well as direct physical harassment of the predator. Although the display behaviors in these communication systems are often well characterized, evidence of the efficacy of these displays in deterring predators is limited due to the challenges associated with studying free‐ranging predators. Here, we examine how the anti‐snake signals of the desert kangaroo rat (Dipodomys deserti) influence the ambush hunting behaviors of sidewinder rattlesnakes (Crotalus cerastes). We found that, although desert kangaroo rats incorporate a number of signal elements into their antipredator display, only sand kicking behavior was a significant factor in motivating sidewinder rattlesnakes to cease hunting: high rates of sand kicking led to early abandonment of ambush coils. These results indicate that anti‐snake displays of small mammals may be especially effective at mitigating the threat posed by rattlesnakes when those displays incorporate physical harassment as well as signaling.     

The origin and dynamic evolution of chemical information transfer

Although chemical communication is the most widespread form of communication, its evolution and diversity are not well understood. By integrating studies of a wide range of terrestrial plants and animals, we show that many chemicals are emitted, which can unintentionally provide information (cues) and, therefore, act as direct precursors for the evolution of intentional communication (signals). Depending on the content, design and the original function of the cue, there are predictable ways that selection can enhance the communicative function of chemicals. We review recent progress on how efficacy-based selection by receivers leads to distinct evolutionary trajectories of chemical communication. Because the original function of a cue may channel but also constrain the evolution of functional communication, we show that a broad perspective on multiple selective pressures acting upon chemicals provides important insights into the origin and dynamic evolution of chemical information transfer. Finally, we argue that integrating chemical ecology into communication theory may significantly enhance our understanding of the evolution, the design and the content of signals in general.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

Evolutionary novelty in communication between the sexes

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.     

Dialog with black box: using Information Theory to study animal language behaviour

In this review, three main experimental approaches for studying animal language behaviour are compared: (1) direct decoding of animals’ communication, (2) the use of intermediary languages to communicate with animals and (3) application of ideas and methods of the Information Theory for studying quantitative characteristics of animal communication. Each of the three methodological approaches has its specific power and specific limitations. Deciphering animals’ signals reveals a complex picture of natural communication in its evolutionary perspective but only fragmentary because of many methodological barriers, among which low repeatability of standard living situations seems to be a bottleneck. Language-training experiments are of great help for discovering potentials of animal language behaviour but leaves characteristics of their natural communications unclear. The use of the methods of Information Theory is based on measuring the time duration that animals spend on transmitting messages of definite information content and complexity. This approach, although does not reveal the nature of animals’ signals, provides a new dimension for studying important characteristics of natural communication systems, which have not been available before. First of all, this approach enables explorers of animals’ language behaviour to obtain knowledge just about the ability of subjects for transferring meaningful messages. Besides, the important properties of animal communication and intelligence can be evaluated such as the rate of information transmission, the complexity of transferred information and potential flexibility of communication systems.     

Functionally referential signals: A promising paradigm whose time has passed

Finding the evolutionary origins of human language in the communication systems of our closest living relatives has, for the last several decades, been a major goal of many in the field of animal communication generally and primate communication specifically. 1 - 4 The so‐called “functionally referential” signals have long been considered promising in this regard, with apparent parallels with the semantic communication that characterizes language. The once‐prominent idea that functionally referential signals are word‐like, in that they are arbitrary sounds that refer to phenomena external to the caller, has largely been abandoned. 5 However, the idea that these signals may offer the strongest link between primate communication and human language remains widespread, primarily due to the fact the behavior of receivers indicates that such signals enable them to make very specific inferences about their physical or social environment. Here we review the concept of functional reference and discuss modern perspectives that indicate that, although the sophistication of receivers provides some continuity between nonhuman primate and human cognition, this continuity is not unique to functionally referential signals. In fact, because functionally referential signals are, by definition, produced only in specific contexts, receivers are less dependent on the integration of contextual cues with signal features to determine an appropriate response. The processing of functionally referential signals is therefore likely to entail simpler cognitive operations than does that of less context‐specific signals. While studies of functional reference have been important in highlighting the relatively sophisticated processes that underlie receiver behavior, we believe that the continued focus on context‐specific calls detracts from the potentially more complex processes underlying responses to more unspecific calls. In this sense, we argue that the concept of functional reference, while historically important for the field, has outlived its usefulness and become a red herring in the pursuit of the links between primate communication and human language. © 2012 Wiley Periodicals, Inc.     

OPTIMAL INVESTMENT IN SOCIAL SIGNALS

This study is an attempt to determine how much individuals should invest in social communication, depending on the type of relationships they may form. Two simple models of social relationships are considered. In both models, individuals emit costly signals to advertise their “quality” as potential friends. Relationships are asymmetrical or symmetrical. In the asymmetrical condition (first model), we observe that low‐quality individuals are discouraged from signaling. In the symmetrical condition (second model), all individuals invest in communication. In both models, high‐quality individuals (elite) do not compete and signal uniformly. The level of this uniform signal and the size of the “elite” turn out to be controlled by the accuracy of signals. The two models may be relevant to several aspects of animal and human social communication.     

The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens

The evolution of signals has mainly been considered in the contextof an emitter-receiver dyadic interaction. However, communicationusually occurs in the presence of individuals (an audience)that are not directly involved in the communication interaction,and it is more realistic to assume that signal evolution occursin a network. Several types of information could be available to an audience, and, therefore, the presence of an audiencecould have effects on the behavior of the communicating animalsand on signal evolution. We investigated whether the presenceof an audience of conspecifics affected intrasexual aggressivecommunication in male fighting fish. We found that if the audiencewas a female, males increased the intensity of conspicuous displays that can be used in communication with both males andfemales and decreased highly aggressive displays that are solelydirected to males. If the audience was a male of similar size,there was no significant change in the way in which males displayed.These results suggest that the presence of an audience couldbe one reason that many long-range and conspicuous signals are often shaped to transmit information to both males and females     

Dragon wars: Movement‐based signalling by Australian agamid lizards in relation to species ecology

It is evident that the environment has the potential to affect animal communication strategies. Species from diverse taxonomic groups using signals from different modalities are known to generate signals that suit the structure of their habitat in order to maximize efficiency. Studies of acoustically communicating species dominate the literature, but visual signals are also tailored to local conditions. There is now increasing evidence that dynamic visual signals, in the form of movement‐based displays, are also influenced by habitat characteristics. Australia's dragon lizards (Family: Agamidae) employ such dynamic signals in a variety of contexts but are particularly common in territory defence. With a few notable exceptions, the signalling behaviour of this group has been relatively overlooked, and the knowledge that does exist is contained in scientific papers focused on other topics or unpublished accounts from herpetologists. In this review, we collated information on the signalling behaviour of these animals and determined that 34 of the 78 species use movement‐based signalling. This number is likely to be an underestimate, as knowledge of the signalling behaviour of many species is lacking. The richly contrasting environments of Australia inhabited by these lizards provide considerable variation in ecological context, so our second objective was to place known signalling behaviour in the context of species ecology. After controlling for phylogeny, we found that broad habitat classifications do not strongly influence the likelihood of motion signalling, and specific motor patterns are not more likely to occur in particular microhabitats. We conclude by suggesting that fully understanding the motion signalling behaviour of Australia's agamids will require documenting the displays of species for which there are no data, while taking into account the high variability existing within motor patterns and considering in detail the environmental context under which signalling takes place.     

Investment in attending to cues and the evolution of amplifiers

Signals and cues are extensively used in social interactions across diverse communication systems. Here, we extend an existing theoretical framework to explore investment by emitters and perceivers in the fidelity with which cues and signals associated with the former are detected by the latter. Traits of the emitter that improve cue or signal fidelity without adding information are termed ‘amplifiers’. We assume that each party can invest in improving fidelity but that it is increasingly costly the more fidelity is improved. Our model predicts that evolution of amplifier traits of a pre‐existing cue occurs over a broader range of circumstances than evolution of signalling in situations where the emitter offered no pre‐existing cue to the perceiver. It further predicts that the greater the intrinsic informational value of a cue, the more likely it is that the perceiver (and not the emitter) will invest in the fidelity of detecting that cue. A consequence of this predicted asymmetry is that true communication with reciprocal adaptations in emitters and perceivers to improve signal fidelity is likely to occur predominantly for traits of intermediate reliability. The corollary is that uncertainty of the perceiver will then be a key feature of communication. Uncertainty can arise because perceivers misinterpret signals or do not perceive them correctly, but here we argue that uncertainty is more fundamentally at the root of communication because traits that are intrinsically highly informative will induce only the perceiver and not the emitter to invest in improved fidelity of perception of that trait.     

Redefining animal signaling: influence versus information in communication

Researchers typically define animal signaling as morphology or behavior specialized for transmitting encoded information from a signaler to a perceiver. Although intuitively appealing, this conception is inherently metaphorical and leaves concepts of both information and encoding undefined. To justify relying on the information construct, theorists often appeal to Shannon and Weaver’s quantitative definition. The two approaches are, however, fundamentally at odds. The predominant definition of animal signaling is thus untenable, which has a number of undesirable consequences for both theory and practice in the field. Theoretical problems include conceptual circularity and running afoul of fundamental evolutionary principles. Problems in empirical work include that research is often grounded in abstractions such as signal honesty and semanticity, and thereby distracted from more basic and concrete factors shaping communication. A revised definition is therefore proposed, making influence rather than transmission of encoded information the central function of animal signaling. This definition is conceptually sound, empirically testable, and inclusive, yet bounded. Implications are considered in both theoretical and empirical domains.     

Different modes of acoustic communication in deep‐diving short‐finned pilot whales (Globicephala macrorhynchus)

Toothed whales use a pneumatic sound generator to produce echolocation and communication sounds. Increasing hydrostatic pressure at depth influences the amplitude and duration of calls but not of echolocation clicks. Here we test the hypothesis that information transfer at depth might be facilitated by click‐based communication signals. Wild short‐finned pilot whales (27) instrumented with multisensor DTAGs produced four main types of communication signals: low‐ and medium‐frequency calls (median fundamental frequency: 1.7 and 2.9 kHz), two‐component calls (median frequency of the low and high frequency components: 2 and 9 kHz), and rasps (burst‐pulses with median interclick interval of 21 ms). Rasps can be confused with foraging buzzes, but rasps are shorter and slower, and are not associated with fast changes in body acceleration nor reduced acoustic output of buzzes, characteristic of prey capture attempts. Contrary to calls, the energy flux density of rasps was not significantly affected by depth. This, and a different information content, may explain the observed increase in the relative occurrence of rasps with respect to calls at depth, and supports the hypothesis that click‐based communication signals may facilitate communication under high hydrostatic pressure. However, calls are produced at depth also, indicating that they may carry additional information relevant for deep‐diving animals, including potential communication among whales diving at the same time in this highly social deep‐diving species.