Semantic communication in birds: evidence from field research over the past two decades

What do animal signals mean? This is a central question in studies on animal communication. Research into the semantics of animal signals began in 1980, with evidence that alarm calls of a non-human primate designated predators as external referents. These studies have challenged the historical assumption that such referential signaling is a unique feature of human language and produced a paradigm shift in animal communication research. Over the past two decades, an increasing number of field studies have revealed similar complexity in anti-predator communication of birds. The acoustic structures of avian alarm calls show a high degree of variation in pitch, duration, shape, and repetition rate. In addition to such distinct and graded variations, several birds combine discrete types of notes or calls into higher complex sequences. These variations in alarm calls are typically associated with the predator’s attributes, such as predator type and distance, and receivers respond to them with appropriate anti-predator behaviors. Although alarm calls of several bird species, as well as those of monkeys, appear to denote predator attributes, almost nothing is known about the cognitive processes that underlie the production and perception of these signals. In this review, I explore the existing evidence for referential signaling in birds and highlight the importance of the cognitive approach to animal communication research. I hope this review will promote further investigations of alarm-calling behavior in birds and will help enhance our understanding of the ecology and evolution of semantic communication.     

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.     

Biases in signal evolution: learning makes a difference

It is now well established that signal receivers have a key role in the evolution of animal communication: the suite of sensory and cognitive processes by which animals perceive and learn about their environment can have a significant impact on signal design. A crucial property of these information-processing mechanisms is the emergence of 'receiver bias' in the behavioural responses to signals. Whereas most research has focussed on receiver biases in the sensory system, more recent studies show that biases can also arise from learning about signals. Here, we highlight how learning-based biases can arise, and how these differ from biases emerging from sensory systems in their impact on signal evolution.     

鸟类社会行为中的嗅觉通讯研究进展

长期以来, 学者普遍认为大多数鸟类的嗅觉能力较弱或丧失。早期实验未能得到统一而清晰的结果, 进一步扩大了这一认知误区。随着研究手段和技术的发展, 解剖学、电生理学、分子生物学和行为生态学等学科提供了鸟类嗅觉存在的证据。目前, 相关研究在鸟类14目33科中发现了嗅觉通讯的证据。与视觉和听觉一样, 这一感觉通路可能在鸟类的觅食、导航、防御、隐蔽、警戒和交流等社会行为中发挥着重要作用。本文着重于嗅觉通讯在鸟类社会行为中的功能, 通过回顾近十年的相关研究, 综述鸟类嗅觉在物种和个体识别、繁殖行为、亲缘识别、配偶选择与竞争等方面发挥的作用。我们也指出: 研究手段的创新将揭示更多鸟类物种在社会行为中对于嗅觉通讯的运用。此外, 当前研究多聚焦于少数物种和单一层面(如生理、生态和环境等), 使用分子生物学、解剖与生理学、行为学和神经生物学手段的整合研究较为缺乏; 而后者更有可能全面地揭示鸟类嗅觉通讯的复杂机理及其在社会行为中发挥的多种功能。     

The different roles of social learning in vocal communication

While vocal learning has been studied extensively in birds and mammals, little effort has been made to define what exactly constitutes vocal learning and to classify the forms that it may take. We present such a theoretical framework for the study of social learning in vocal communication. We define different forms of social learning that affect communication and discuss the required methodology to show each one. We distinguish between contextual and production learning in animal communication. Contextual learning affects the behavioural context or serial position of a signal. It can affect both usage and comprehension. Production learning refers to instances where the signals themselves are modified in form as a result of experience with those of other individuals. Vocal learning is defined as production learning in the vocal domain. It can affect one or more of three systems: the respiratory, phonatory and filter systems. Each involves a different level of control over the sound production apparatus. We hypothesize that contextual learning and respiratory production learning preceded the evolution of phonatory and filter production learning. Each form of learning potentially increases the complexity of a communication system. We also found that unexpected genetic or environmental factors can have considerable effects on vocal behaviour in birds and mammals and are often more likely to cause changes or differences in vocalizations than investigators may assume. Finally, we discuss how production learning is used in innovation and invention, and present important future research questions. Copyright 2000 The Association for the Study of Animal Behaviour.     

Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics

The evolution of the complex and dynamic behavioural interactions between caring parents and their dependent offspring is a major area of research in behavioural ecology and quantitative genetics. While behavioural ecologists examine the evolution of interactions between parents and offspring in the light of parent-offspring conflict and its resolution, quantitative geneticists explore the evolution of such interactions in the light of parent-offspring co-adaptation due to combined effects of parental and offspring behaviours on fitness. To date, there is little interaction or integration between these two fields. Here, we first review the merits and limitations of each of these two approaches and show that they provide important complementary insights into the evolution of strategies for offspring begging and parental resource provisioning. We then outline how central ideas from behavioural ecology and quantitative genetics can be combined within a framework based on the concept of behavioural reaction norms, which provides a common basis for behavioural ecologists and quantitative geneticists to study the evolution of parent-offspring interactions. Finally, we discuss how the behavioural reaction norm approach can be used to advance our understanding of parent-offspring conflict by combining information about the genetic basis of traits from quantitative genetics with key insights regarding the adaptive function and dynamic nature of parental and offspring behaviours from behavioural ecology.     

Brain evolution by brain pathway duplication

Understanding the mechanisms of evolution of brain pathways for complex behaviours is still in its infancy. Making further advances requires a deeper understanding of brain homologies, novelties and analogies. It also requires an understanding of how adaptive genetic modifications lead to restructuring of the brain. Recent advances in genomic and molecular biology techniques applied to brain research have provided exciting insights into how complex behaviours are shaped by selection of novel brain pathways and functions of the nervous system. Here, we review and further develop some insights to a new hypothesis on one mechanism that may contribute to nervous system evolution, in particular by brain pathway duplication. Like gene duplication, we propose that whole brain pathways can duplicate and the duplicated pathway diverge to take on new functions. We suggest that one mechanism of brain pathway duplication could be through gene duplication, although other mechanisms are possible. We focus on brain pathways for vocal learning and spoken language in song-learning birds and humans as example systems. This view presents a new framework for future research in our understanding of brain evolution and novel behavioural traits.     

A decadal review of urban ornithology and a prospectus for the future

The study of urban birds has increased exponentially in the last century. A prior review of the scientific literature up to the year 2000 found 100 research articles on urban birds, but in the past decade alone, over 1000 have been published. Here I review the studies from 2006–2015 to characterize their approach, location, general findings and recent obsessions, with an eye toward suggesting important future directions. Urban ornithology remains centred in the northern hemisphere, although there is a rapid increase in studies from southern, tropical and biodiverse settings. Studies in the north have changed from documentation of the composition of urban avifaunas to include many studies of the demographic response to aspects of urban environments. Studies of pattern remain most common in Latin America, Asia, Africa, New Zealand and the Middle East. Across the world, ornithologists are revealing the rapid evolution of behavioural and morphological adaptations by birds to the urban environment, much of which is due to phenotypic plasticity. The relationship of humans to nature generally and birds specifically has been increasingly studied as a driver of avifaunal change as well as a factor affecting human ethics. Urban ornithology remains rarely experimental, but it has matured to the point of supporting synthetic reviews and meta‐analyses that quantify the loss of avian diversity from city centres, characterize successful urban birds, discuss the role of amount and arrangement of vegetation on bird life, and explore the complex relationships between the subsidies and hazards of urban life and the survival and reproduction of birds. Yet much remains to be learned, including how some species thrive in cities with abundant predators; how city form and location affect the peak in avian richness that occurs typically at intermediate levels of urbanization; the significance of functional biotic homogenization; and the ways in which engaging citizens in urban bird life informs their broader environmental land ethic.     

The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates

Vertebrates represent one of the best-studied groups in terms of the role that mating preferences have played in the evolution of exaggerated secondary sexual characters and mating behaviours within species. Vertebrate species however, also exhibit enormous interspecific diversity in features of mating signals that has potentially led to reproductive isolation and speciation in many groups. The role that sexual selection has played in interspecific divergence in mating signals has been less fully explored. This review summarizes our current knowledge of how mating preferences within species have shaped interspecific divergence in mate recognition signals among the major vertebrate groups. Certain signal modalities appear to characterize mating signal diversification among different vertebrate taxa. Acoustic signals play an important role in mating decisions in anuran amphibians and birds. Here, different properties of the signal may convey information regarding individual, neighbor and species recognition. Mating preferences for particular features of the acoustic signal have led to interspecific divergence in calls and songs. Divergence in morphological traits such as colouration or ornamentation appears to be important in interspecific diversity in certain groups of fishes and birds. Pheromonal signals serve as the primary basis for species-specific mating cues in many salamander species, most mammals and even some fishes. The evolution of interspecific divergence in elaborate courtship displays may have played an important role in speciation of lizards, and particular groups of fishes, salamanders, birds and mammals. While much research has focused on the importance of mating preferences in shaping the evolution of these types of mating signals within species, the link between intraspecific preferences and interspecific divergence and speciation remains to be more fully tested. Future studies should focus on identifying how variation in mating preferences within a species shapes interspecific diversity in features of mating signals in order to better understand how sexual selection may have led to speciation in vertebrates.     

Behavioural divergence,interfertility and speciation: A review

Behavioural compatibility between mates is fundamental for maintaining species boundaries and is achieved through appropriate communication between males and females. A breakdown in communication will lead to behavioural divergence and reduced interfertility. In this review, we summarise the current knowledge on male signals and female perception of these signals, integrating the literature from several taxa. We advocate that signaller–perceiver coevolution, which is usually under strong stabilising selection to enable mating, forms the basis of species-specific mate recognition systems. The mechanisms (phylogeny, geography, ecology, biology) shaping signaller–perceiver systems are briefly discussed to demonstrate the factors underpinning the evolution of signaller–perceiver couplings. Since divergence and diversification of communication systems is driven by changes in the mechanical properties of sensory pathways and morphology of sensory organs, we highlight signal modalities (auditory, olfactory, visual, tactile) and their importance in communication, particularly in mate selection. Next, using available examples and generating a stylised model, we suggest how disruption (biological, ecological, stochastic) of signaller–perceiver systems drives behavioural divergence and consequently results in reduced interfertility and speciation. Future studies should adopt an integrative approach, combining multiple parameters (phylogeny, adaptive utility of communication systems, genetics and biomechanical/biochemical properties of signals and perception) to explore how disruption of signaller–perceiver systems results in behavioural divergence and reduced interfertility. Finally, we question the impact that rapid environmental change will have on disruption of communication systems, potentially interfering with signaller–perceiver couplings.     

The behavioural ecology of marine cleaning mutualisms

Cleaning interactions, in which a small ‘cleaner’ organism removes and often consumes material from a larger ‘client’, are some of the most enigmatic and intriguing of interspecies interactions. Early research on cleaning interactions canonized the view that they are mutualistic, with clients benefiting from parasite removal and cleaners benefiting from a meal, but subsequent decades of research have revealed that the dynamics of these interactions can be highly complex. Despite decades of research on marine cleaning interactions (the best studied cleaning systems), key questions remain, including how the outcome of an individual cleaning interaction depends on ecological, behavioural, and social context, how such interactions arise, and how they remain stable over time. Recently, studies of marine parasites, long-term data from coral reef communities with and without cleaners, increased behavioural observations recorded using remote video, and a focus on a larger numbers of cleaning species have helped bring about key conceptual advances in our understanding of cleaning interactions. In particular, evidence now suggests that the ecological, behavioural, and social contexts of a given cleaning interaction can result in the outcome ranging from mutualistic to parasitic, and that cleaning interactions are mediated by signals that can also vary with context. Signals are an important means by which animals extract information about one another, and thus represent a mechanism by which interspecific partners can determine when, how, and with whom to interact. Here, I review our understanding of the behavioural ecology of marine cleaning interactions. In particular, I argue that signals provide a useful framework for advancing our understanding of several important outstanding questions. I discuss the costs and benefits of cleaning interactions, review how cleaners and clients recognize and assess one another using signals, and discuss how signal reliability, or ‘honesty’, may be maintained in cleaning systems. Lastly, I discuss the sensory ecology of both cleaners and clients to highlight what marine cleaning systems can tell us about signalling behaviour, signal form, and signal evolution in a system where signals are aimed at multiple receiver species. Overall, I argue that future research on cleaning interactions has much to gain by continuing to shift the research focus toward examining the variable outcomes of cleaning interactions in relation to the broader behavioural, social, and ecological contexts.     

Behavioural,ecological, and evolutionary aspects of diversity in frog colour patterns

The role of colours and colour patterns in behavioural ecology has been extensively studied in a variety of contexts and taxa, while almost overlooked in many others. For decades anurans have been the focus of research on acoustic signalling due to the prominence of vocalisations in their communication. Much less attention has been paid to the enormous diversity of colours, colour patterns, and other types of putative visual signals exhibited by frogs. With the exception of some anecdotal observations and studies, the link between colour patterns and the behavioural and evolutionary ecology of anurans had not been addressed until approximately two decades ago. Since then, there has been ever‐increasing interest in studying how colouration is tied to different aspects of frog behaviour, ecology and evolution. Here I review the literature on three different contexts in which frog colouration has been recently studied: predator–prey interactions, intraspecific communication, and habitat use; and I highlight those aspects that make frogs an excellent, yet understudied, group to examine the role of colour in the evolution of anti‐predation strategies and animal communication systems. Further, I argue that in addition to natural‐history observations, more experiments are needed in order to elucidate the functions of anuran colouration and the selective pressures involved in its diversity. To conclude, I encourage researchers to strengthen current experimental approaches, and suggest future directions that may broaden our current understanding of the adaptive value of anuran colour pattern diversity.     

一种泡蟾的配偶识别:脑、行为和进化研究

综述了对泡蟾(Physalaemuspus pustulosus)的性通讯所进行的各种研究。本文作者研究了通讯系统的功能重要性、通讯的神经机制以及通讯进化的格局,特别研究了雌蛙如何使用简单和复杂的叫声来识别可以交配的物种,以及如何识别同种的不同雄性个体。本文确定了复杂叫声的反选择力、一种食蛙蝠——缨唇蝠(Trachops cirrhosus)以及叫声的能量消耗,并阐述了引起雌性反应的重要特征。作者的比较研究表明,对复杂叫声的偏好在复杂叫声进化前就有了,这支持感官开发假说(Hypothesis of sensory exploitation,雄性特征进化的结果是开发雌性预先存在的对雄性的偏好)。结合比较研究和人工神经网络的模拟,作者认为雌蛙用来识别雄性简单叫声的解码策略受其祖先解码策略的影响[动物学报49(6)：713～726,2003]。     

Intentional communication: solving methodological issues to assigning first-order intentional signalling

Intentional signalling plays a fundamental role in human communication. Mapping the taxonomic distribution of comparable capacities may thus shed light on the selective pressures that enabled the evolution of human communication. Nonetheless, severe methodological issues undermine comparisons among studies, species and communicative modalities. Here, we discuss three main obstacles that hinder comparative research of ‘first-order’ intentional signalling (i.e. voluntary signalling in pursuit of a cognitively represented goal): (i) inconsistency in how behavioural hallmarks are defined and operationalised, (ii) testing of behavioural hallmarks without statistical comparison to control conditions, and (iii) bias against the publication of negative results. To address these obstacles, we present a four-step scheme with 20 statistical operational criteria to distinguish between non-intentional and first-order intentional signalling. Our unified scheme applies to visual and audible signals, thereby validating comparison across communicative modalities and species. This, in turn, promotes the generation and testing of hypotheses about the evolution of intentional communication.     

鸟类线粒体DNA研究概述

线粒体DNA作为理想的分子标记已被广泛用于鸟类种群遗传学和进化遗传学的研究,并取得了许多有意义的结果。本文介绍鸟类线粒体DNA的组成、结构特点及多态性的研究,综述近年来有关鸟类分子进化研究的进展情况,对今后的发展进行了初步的探讨。 Abstract:Mitochondrial DNA as a genetic marker has been successfully applied to the study of molecular evolution of birds.The apparently maternal inheritance of mitochondrial DNA and its fast evolution in primary sequence has made it attractive in population and evolutionary genetics.Mitochondrial DNA of birds displays two characteristics not seen in other vertebrates mtDNA,that is,a novel gene order and the absence of an equivalent to the light-strand replication origin.The research on polymorphism of mtDNA can resolve phylogenies of birds both at lower and higher taxonomic levels.Here we review progress on avian molecular evolution in recent years,and make preliminary studies of the development in this field.     

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.     

Ecology and genetics of speciation in Ficedula flycatchers

Birds have for long been popular study objects in speciation research. Being easy to observe in the field, they have traditionally been particularly important in studies of behavioural and ecological factors in speciation, whereas the genetic aspects of the process have been studied in other organisms, such as Drosophila. More recently, however, a stronger genetic focus has been placed on speciation research also in birds. Here, we review ecological, behavioural and genetic studies on speciation in the pied flycatcher (Ficedula hypoleuca) and the collared flycatcher (Ficedula albicollis). These well‐studied birds provide among the few proposed examples of the process of reinforcement of premating isolation, and the evidence for reinforcement is strong. They are further characterized by having strong intrinsic postzygotic barriers (female hybrid sterility), yet the two species appear to be very similar ecologically. This is in stark contrast to another well‐studied bird complex, Darwin’s finches, in which the species differ vastly in ecologically important traits but have no developmental problems arising from genetic incompatibilities, and where no evidence for reinforcement is found. In the flycatchers, sex chromosome linkage of genes affecting traits associated with both pre‐ and postzygotic barriers to gene exchange is likely to facilitate reinforcement. We discuss whether such sex‐linkage may be common in birds. The contrast between flycatchers and Darwin’s finches indicate that speciation in birds cannot always be understood mainly as a result of divergent natural selection (‘ecological speciation’), and generalizations from one system may lead us astray. We discuss to what extent insight from research on the flycatchers may point to fruitful avenues for future research on bird speciation and specifically call for a more systematic effort to simultaneously investigate ecology, behaviour and genetics of birds caught in the process of speciation.     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

鸟类对城市化的适应

城市生态系统是以人为主导的复杂系统,当前的高速城市化进程对包括鸟类在内的城市区域动物施加了广泛的选择压力。从鸟类对城市环境的主动适应角度,归纳了国内外城市鸟类生态学研究中有关鸟类对城市化的适应研究,探讨了城市化进程中城市鸟类行为、生理指标以及种群基因结构的适应性变化。基于遗传的数量效应,研究认为某些鸟种对城市环境的适应已经上升到进化层次,同时还对城市化导致鸟类新物种形成的可能性进行了探讨。最后,对鸟类对城市化适应的研究前景提出了展望。     

Feather function and the evolution of birds

The ability of feathers to perform many functions either simultaneously or at different times throughout the year or life of a bird is integral to the evolutionary history of birds. Many studies focus on single functions of feathers, but any given feather performs many functions over its lifetime. These functions necessarily interact with each other throughout the evolution and development of birds, so our knowledge of avian evolution is incomplete without understanding the multifunctionality of feathers, and how different functions may act synergistically or antagonistically during natural selection. Here, we review how feather functions interact with avian evolution, with a focus on recent technological and discovery-based advances. By synthesising research into feather functions over hierarchical scales (pattern, arrangement, macrostructure, microstructure, nanostructure, molecules), we aim to provide a broad context for how the adaptability and multifunctionality of feathers have allowed birds to diversify into an astounding array of environments and life-history strategies. We suggest that future research into avian evolution involving feather function should consider multiple aspects of a feather, including multiple functions, seasonal wear and renewal, and ecological or mechanical interactions. With this more holistic view, processes such as the evolution of avian coloration and flight can be understood in a broader and more nuanced context.