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1 - Animal Communication Overview

from Part I - Communication and Language

Published online by Cambridge University Press:  01 July 2021

Allison B. Kaufman
Affiliation:
University of Connecticut
Josep Call
Affiliation:
University of St Andrews, Scotland
James C. Kaufman
Affiliation:
University of Connecticut

Summary

This chapter provides a broad overview of terminology and concepts in the study of animal communication. First, we focus on the evolutionary origins or phylogenetic causes of communicative signals. We address how communication systems can arise under several circumstances by increasing the reproductive success of both senders and receivers of signals. We summarize terminology describing what is communicated (self-reporting and other-reporting), how it is communicated (different modalities) and to whom it is communicated (conspecifics, heterospecifics). We further discuss how signal design is influenced by the risk of deception. The debate between the information and manipulation perspective of animal communication is briefly outlined. The second part of the chapter focuses on proximate aspects of animal communication. We describe signal acquisition in animals through ultimate mechanisms (biological inheritance, phylogenetic ritualization) and proximate mechanisms (ontogenetic ritualization, cultural learning) with a particular focus on learning. We further discuss signal selection, i.e., to what degree some animals have flexible control over signals and how they adjust them according to the recipient. Last, we discuss new directions and open questions in the study of animal communication, i.e., considerations of compositionality and multimodality, turn-taking, repertoire acquisition and development, flexibility and memory, and the problem of using a one-size-fits-all approach for understanding animal communication systems.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2021

For one reason or another, you have decided to pick up this book. Assuming that you are reading the printed words and understand English, your motivation to do so is likely to acquire information about the topic displayed on the cover: animal cognition. If you want to show this chapter to your pet, they might perceive similar visual stimuli – black symbols on a white page – however, they will not extract the same information as you can. Many human societies have developed writing as a cultural tool that allows transmitting linguistic information beyond the present to a theoretically unlimited number of individuals who are able to read the content. Acquiring the skills necessary for reading and writing is a time-consuming process, and does not come easily to us; mastering this practice takes many years. On an evolutionary scale, representing language through written symbols is a relatively recent invention, and still accounts for only a fraction of the information that we communicate with each other. Notably, our ability to read written symbols relies on cortical areas of the brain that have evolved for object and face visual recognition and clearly not for reading per se (see e.g., Dehaene & Cohen, Reference Dehaene and Cohen2011). Spoken language, in contrast, is not only considerably older, but also a human universal and commonly listed as one of the defining abilities of our species. Language enables us to flexibly communicate feelings and ideas with innumerable degrees of freedom. While a communication system as complex as language might be unique to our species, the transfer of information between organisms is a common phenomenon in biology. The study of communication across the phylogenetic tree can not only help to better understand how human language has evolved but is also central to understanding living organisms in general. Depending on the definition, communication is not limited to animal species, but can be found across a wide spectrum of species, such as bacteria and plants. Even communication between different biological kingdoms can be commonly found, and is the subject of a rich body of research literature, for example plant–animal communication (e.g., Schaefer & Ruxton, Reference Schaefer and Ruxton2011). This is, however, beyond the scope of this chapter, which will rather provide a brief summary of concepts, approaches, and issues related to the study of communication between animals.

It is important to note that animal communication, like every other biological phenomenon, can be addressed on multiple levels. The most common framework for explaining behavior on different (but complementary) levels of analyses are Tinbergen’s four questions. In his seminal paper On aims and methods of Ethology, the Dutch ornithologist and ethologist Nikolaas Tinbergen (Reference Tinbergen1963) distinguished between causation, ontogeny, adaptation, and phylogeny. Causation and ontogeny can be grouped as proximate, or how, questions. Explanations of causation address mechanistic explanations of behaviors, that is, they address the question: “How does it work?” For example, how do certain muscle movements bring about observable behavior? Ontogeny refers to the development over the lifespan of an individual and thus addresses how a behavior develops and changes over the life course of an animal. Proximate questions can theoretically be observed by studying one individual longitudinally. In contrast, adaptation and phylogeny are categorized as ultimate. or why, questions, that is, questions that relate to the evolutionary origins of behaviors. These questions, therefore, address evolutionary timescales across many generations. The question of adaptation asks if and how certain behaviors have contributed to the reproductive success (i.e., the likelihood of producing viable offspring) of an individual’s ancestors. Colloquially, adaptation inquiries could be translated into the question: “What is it good for?” Given that evolution through natural selection operates through making gradual changes to preexisting structures, the question of phylogeny addresses precursors and origins of the phenomena under question in the ancestral lineage of an organism by asking the question, “Where did it come from?”

We broadly divide this chapter into two sections. First, we focus on ultimate explanations for animal communication. Then, we continue with some proximate explanations for animal communication. Historically, the study of animal communication started with a focus on the phylogeny of animal communication, but in recent years proximate mechanisms have received increasing attention.

Why Do Animals Communicate? (Ultimate Explanations)

We start by briefly outlining some ultimate explanations (evolutionary causes) as to why animals communicate with each other in the first place. In general, natural selection can produce organisms with perceptive and cognitive skills that enable them to acquire information about their environment. Obtaining information about the environment through phylogenetic and ontogenetic processes allows organisms to behave in ways that increase their chances for survival and reproduction. Through adaptations to the environment, natural selection thus produces organisms that indirectly represent properties of the external world that affected the reproductive success of their ancestors. Lorenz, for example (Reference Lorenz1941, Reference Lorenz1973), illustrated this process through his example of the evolution of the fins of a fish. Over the course of phylogeny, fins were shaped by the physical properties of water, and thus contain information about water that was relevant for the survival of the ancestral lineage of fish. The properties of water are a stable aspect in the environment of many aquatic animals, therefore structures analogous to fins that enable moving efficiently in water can be found across many species, such as cetaceans and penguins. The degree to which aspects of an organism’s environment remain stable throughout phylogeny and ontogeny are related to the nature of adaptations. Environmental properties that remain stable across phylogeny can be matched by adaptations that require little flexibility, whereas less stable properties of the environment might require more flexible adaptations in the form of physiology, perception, cognition, and behavior. The behavior of other organisms – both conspecifics and different species – is an influential environmental factor for most animals, which exerts great influence over their reproductive success. Because the behavior of organisms can influence each other, many of their relationships can be bidirectional and will therefore create positive feedback loops on their evolution. Note that the relationship between certain physical aspects of an environment and an organism might only be unidirectional. Take the example of aquatic animals and water – while the properties of water affected their evolution, the same is not true for the opposite direction. However, organisms can adapt to each other’s behavior through both phylogenetic and ontogenetic mechanisms. The relationship is therefore often bidirectional and can lead to evolutionary arms races (Dawkins & Krebs, Reference Dawkins and Krebs1979). Dynamics like these have been extensively documented and researched in animal communication.

One of the first systematic studies of animal communication was developed within the field of ethology, which mainly focused on the phylogeny, the ancestral origins of communicative behaviors. For example, Konrad Lorenz was interested in reconstructing the phylogeny of behaviors by focusing on display patterns (e.g., threats and courtship displays) across different species. While behaviors themselves do not fossilize, comparing behavior patterns of extant species is one way of tracking phylogenetic relationships through homologies. This behavioral approach allows reconstructing shared ancestral behaviors across animal species. One of the reasons Lorenz focused on communicative, ritualized behaviors was their conspicuous nature. According to Lorenz (Reference Lorenz1966), one of the most important characteristics of a phylogenetically ritualized behavior is that a motor pattern that originally served a noncommunicative function in the environment changed in a way that it also served a new communicative function. This is similar to Tinbergen’s (Reference Tinbergen1952) work on derived activities, which drew on insights from his extensive work with birds. Much of Lorenz’s research on animal communication focused on backtracing the behaviors and motivational conflicts that eventually led to the development of communicative signals. According to him, many signals initially evolved from intention movements, that is, movements that precede a behavior, or displacement activities, behaviors that are performed as a result of opposing motivational drives (e.g., fighting vs. fleeing).

More broadly, most organisms have to acquire information about their physical and animate environment throughout their lifetime in order to survive and reproduce. Danchin and colleagues (Reference Danchin, Giraldeau, Valone and Wagner2004) divide the information that individuals acquire about their environment into personal information and social information. Personal information refers to information that an animal individually acquires about its environment, for example through direct perception of, and interaction with, the physical world, like trial-and-error-learning. In contrast, social information refers to all information acquired through observing other organisms. Social information can be about the physical environment, or about properties and states of other organisms. Social information can be further categorized into cues and signals. Cues are also referred to as inadvertent social information because they are not shaped by natural selection to be picked up by other organisms. Nonetheless, they might be picked up by others, which might result in negative, neutral, or positive outcomes for the cue producer. For example, imagine yourself walking down a muddy trail. On your way, you encounter bear tracks in the mud. This is a cue that might lead you to change your walking direction in order to prevent an unwelcomed encounter with a bear. However, the bear’s tracks are just a by-product created by its movement through the muddy terrain, and are not left by the bear in order to be perceived by you. Generally, both the ultimate and proximate reasons for the occurrence of cues do not involve providing information to others. Instead, the information that might get picked up is simply a by-product of other activities. In contrast, animal signals are acts or structures that evolved for the “specific purpose of conveying information and thereby influencing others’ behavior, ultimately impacting both the signaler’s and the recipient’s fitness” (Laidre & Johnstone, Reference Laidre and Johnstone2013, R831). Therefore, animal communication occurs when a sender transmits a signal with the goal of influencing the behavior of at least one receiver. Many signals originated from acts or structures that once were cues. It is possible for cues to evolve into signals if they – on average – provide benefit for both the sender and the receiver (Laidre & Johnstone, Reference Laidre and Johnstone2013). Signal design is always the outcome of a bidirectional relationship, meaning it is influenced by the selective pressure applied to both the signaler and the receiver (Johnstone, Reference Johnstone, Krebs and Davies1997).

Signals can further be distinguished based on the kind of information that is communicated. Maynard Smith and Harper (Reference Smith and Harper1995) distinguish between self-reporting signals, which “provide information, positive or negative, about some property of the signaller” and other-reporting signals, which provide “information about an object or organism other than the signaller” (p. 307). Warning coloration, also referred to as aposematism, is one example of a self-reporting signal that can be found in many prey species that protect themselves against predators by producing poison. Not only does the poisonous prey benefit from not getting eaten, but the predator also benefits from not getting poisoned. Therefore, selective pressure is put on both individuals to establish a signal that prevents this from happening. The prey species therefore benefits from exploiting the predator’s vision and psychology in order to generate a conspicuous warning coloration that can easily be recognized (Stevens & Ruxton, Reference Schaefer and Ruxton2011). For example, many poison frogs (Dendrobatidae) have conspicuous coloration and patterns on their bodies that are meant to be detected by potential predators (Santos, Coloma, & Cannatella, Reference Santos, Coloma and Cannatella2003; Darst, Cummings, & Cannatella, Reference Darst, Cummings and Cannatella2006). In contrast, alarm calls are an example of an other-reporting signal that can be found in many mammal and bird species. Some of these gregarious animal species will produce calls that inform conspecifics about the presence of predators. One well-studied example is the alarm calls produced by vervet monkeys (Cercopithecus aethiops). Notably, these primates do not only produce one type of alarm call, but instead will produce different alarm calls associated with the detection of different predators, such as leopards, snakes, and hawks. Each call will elicit a different fleeing response in the monkeys that is appropriate for avoiding attacks by specific predators (Seyfarth, Cheney, & Marler, Reference Seyfarth, Cheney and Marler1980). For example, the monkeys respond to the leopard alarm call of conspecifics by seeking shelter in trees.

The examples of alarm calls and warning coloration illustrate that signals can develop within cooperative relationships, such as informing conspecifics with alarm calls, but also within competitive contexts, such as warning colorations that are meant to deter predators. In order to be effective, signals should be designed in a way that they can be easily detected, discriminated, and remembered by receivers (Guilford & Dawkins, Reference Guilford and Dawkins1991). In other words, efficient signals can decrease the perceptual threshold and cognitive effort that is needed by the receiver to pick up information. Therefore, communication can package information in a more accessible way through both reducing the perceptual threshold and the cognitive effort of receivers to gain access to information about their environment. Notably, this highlights that signals are not optimized to transmit information in absolute terms, but rather in the most accessible way based on the perceptual and cognitive systems of the receiver. This can explain why many signals contain redundancy and make use of different modalities simultaneously.

There is a great diversity of perceptual abilities across the animal kingdom, corresponding to a broad range of modalities that are used for transmission. Bradbury and Vehrencamp (Reference Bradbury and Vehrencamp1998) provide a detailed overview and discussion on the mechanics and different modalities associated with signal transmission in animals, for example through auditory, visual, and chemical channels. Signals vary widely in their duration, oftentimes associated with the medium through which they are transferred. While acoustic signals, such as alarm calls, might be highly transient and fleeting, other signals, such as the warning colorations against predators, can be inflexible and enduring throughout most of the life of the signaler. Moreover, signals tend to be produced with a typical intensity and a typical frequency or duration, so as to facilitate recognition and reduce signal ambiguity (Morris, Reference Morris1957). Flexibility and variability occur in special situations that require the production of signals louder, longer or more often, for example to convey urgency or danger. Imagine somebody calling your name to summon you to do something, and under which conditions they would be calling you more loudly (e.g., because of urgency or because you seem distracted) or more softly than usual (e.g., to make the summoning less public, possibly to hide it from possible overhearers).

The signals used for alarm calls and warning coloration do not only differ with regard to their durations, but also with regard to the relationship with the receiver. While some are directed towards conspecifics, for example courtship displays, others can be directed towards members of different species, such as in the example of warning coloration against potential predators. According to signaling theory, signals can emerge as long as they provide, on average, benefits to both the signaler and the receiver, regardless of the nature of the relationship. One striking example for interspecific communication is the symbiotic relationship between humans and greater honeyguides (Indicator indicator). These birds can be found in sub-Saharan Africa and acquired their name from their ability to lead humans (such as the Boran people of Kenya) to bees’ nests. Honeyguides produce acoustic and visual signals to inform humans about the location of bees’ nests that they have spotted. Both parties mutually benefit from this relationship (Isack & Reyer, Reference Isack and Reyer1989). Honey gatherers reduce their time searching for bees’ nest when they are being guided by the honeyguide. In return, the birds gain easier access to the beeswax and larvae and have a reduced risk of getting stung by bees, because the humans use fire during the extraction of honey. Both humans and honeyguides produce specific calls during the honey search that are recognized by the other species (Spottiswoode, Begg, & Begg, Reference Spottiswoode, Begg and Begg2016). This symbiotic signal exchange is possible because the auditory perceptual spectra of humans and honeyguides overlap sufficiently to recognize each other’s calls.

However, not every relationship between senders and receivers with overlapping perceptual spectra ends up being symbiotic. Animals can also “listen into” calls produced by third parties in order to gain social information. Eavesdropping occurs when organisms use cues or signals from other organisms to their benefit for which they are not the intended receivers (Bradbury & Vehrencamp, Reference Bradbury and Vehrencamp1998) and thus is a form of social information. Therefore, the extent to which producing a signal is beneficial to the signaler is not only based on the responses of intended receivers, but also potentially by the responses and behaviors of eavesdroppers. As such, selective pressure on the design of signals is not only a result of the interaction between senders and receivers, but also based on the responses by eavesdroppers. If senders produce signals that would commonly be used by eavesdropping predators to locate them, the risks of producing the signal might exceed the potential benefits for the sender. However, eavesdropping does not necessarily result in negative consequences for senders or receivers. For example, Potvin and colleagues (Reference Potvin, Ratnayake, Radford and Magrath2018) showed that wild-superb fairy-wens (Malurus cyaneus) can learn to associate alarm calls from other species with predators through acoustic learning when they co-occur with alarm calls with which they were already familiar. Wild superb fairy-wrens therefore eavesdrop on other species’ alarm calls, which is not necessarily disadvantageous for the heterospecific callers. Eavesdroppers can be both individuals from the same species as the sender of the signal and individuals from different species, such as the example with the fairy-wrens described. In the case of eavesdropping, an animal intercepts the communication between third-party senders and receivers. In principle, the fitness consequences can be on average positive, negative, or neutral for the intercepted parties.

Additionally, animal communication systems are also vulnerable to deception, both within and between species. Animals may find themselves in a broad range of situations in which the production of and response to a signal is beneficial to them but not necessarily the receiver. According to Searcy and Nowicki (Reference Searcy and Nowicki2005) (who use a slightly modified definition by Mitchell (Reference Mitchell, Mitchell and Thompson1986)) deception occurs when a “receiver registers something Y from a signaler; the receiver responds in a way that benefits the signaler and is appropriate if Y means X; and it is not true that X is the case” (p. 5). For example, female fireflies of several Photuris species mimic the sexual flash signals of females from other firefly species, for example, Robopus and Photinus, in order to lure in males from those species and prey on them (Lloyd, Reference Lloyd1983; El-Hani, Queiroz, & Stjernfelt, Reference El-Hani, Queiroz and Stjernfelt2010). The males register what they interpret as a sexual signal by female conspecifics, and therefore approach the flash signal, which would be an appropriate (i.e., adaptive) response if it were indeed produced by a female of their own species and not a deception by another species of fireflies. Another example of deception can be found in brood parasites, with the most famous example being the cuckoo (Cuculus canorus), but also some species of the previously mentioned honeyguide. Brood parasitism substantially reduces costs of parental investment: The females of the parasite species lay their eggs in the nests of other species. If the brood parasite succeeds, the host species will feed and raise the hatched chick as their own. The fact that animal communication systems can be susceptible to deception raises the question of how reliable signals can persist nonetheless, particularly in situations where a sender could derive benefits from deceiving. Zahavi (Reference Zahavi1975) provided one possible answer, by introducing his concept of honest signals along with the notion of the handicap principle. According to this view, signals that are costly to the signaler, and thus cannot effortlessly be produced (they constitute a handicap for the signaler), can be considered “honest.” Through increased costs, the signals become less likely to be deceptive because the reproduction costs would be higher than the gains of faking it.

Signals can be costly in different ways, such as the amount of effort needed to produce them, the increased likelihood of detection by individuals other than the target recipient, or by the handicap they impose on the signaler. Grafen (Reference Grafen1990) expanded on Zahavi’s handicap principle by developing mathematical models that show that honest signaling can become an evolutionary stable strategy. Searcy and Nowicki (Reference Searcy and Nowicki2005) suggest the following criteria for a reliable signal: “1. Some characteristic of the signal (including, perhaps, its presence/absence) is consistently correlated with some attribute of the signaler or its environment; and 2. Receivers benefit from having information about this attribute” (p. 3). Thus, receivers influence the evolution of signals by selectively responding to them.

What Are Signals for?

Contrary to the classical ethological position, which focused more on physiological adaptations and generally avoided claims about animals’ “minds,” an important perspective in the study of animal communication that gained momentum in the late 1970s is the information perspective. It heavily relies on the Shannon and Weaver’s model of communication (Reference Shannon and Weaver1949), which defines information as the reduction of uncertainty in the receiver and on Wiener’s (Reference Wiener1948) cybernetic theory of communication and feedback control. The idea is that communication consists of encoding and decoding information via the production and perception of signals. To that degree, it is possible to map the meaning of signals, and a signal could be assessed in terms of its honesty (Zahavi, Reference Zahavi1975), that is, in terms of how it reflects specific characteristics of the signaler or its intentions. Signals encode information and the main task of the perceiver is to decode the signal. Note that in its basic form, the theory claims that if there is a predictable relation between the occurrence of a signal (e.g., an alarm call) and the occurrence of a specific stimulus or social situation (e.g., a predator), then the listener can use the signal to infer what is happening or predict what is going to happen. As such, a large amount of effort has been spent in trying to assess to what degree the occurrence of a signal predicts or is associated with either something about the world of relevance for the recipient (e.g., presence of food, danger, identity of the signaler) or what the signaler might be doing next (e.g., initiating an aggression).

The information perspective took hold and became more dominant with the advent of the cognitive revolution and the use of computational metaphors to describe animal communication. Marler (Reference Marler1961) was one of the first scholars to propose that animal signals were adaptive because they were providing listeners with information. He was particularly focused on primates’ vocal productions at a time when the general consensus was that they were mostly involuntary reflexes evoked by highly arousing emotional situations. Yet his insight was that signals had to be necessarily more flexible than generally established in the laboratory, or that they at least required some form of contextual processing, because of the highly complex social environments that primates are living in. The claim was that in natural settings, independently of whether they were produced voluntarily or intentionally, signals had to provide listeners with valuable information (Marler, Reference Marler, DeVore and Hall1965). Along the same lines, Smith (1977) highlighted the importance of contextual cues in the recipient’s processing of a signal by famously suggesting that there cannot be some simple one-to-one signal mapping, but rather perceivers have to invest processing effort to interpret the signals they are exposed to. The discovery that vervet monkey alarm calls might have clear semantic meanings (Seyfarth et al., Reference Seyfarth, Cheney and Marler1980) provided further strength to a perspective aimed at unpacking the meaning of animal signals and that believed in the possibility of developing species typical lexicons, especially for nonhuman primates (Zuberbühler, Reference Zuberbühler2000a, Reference Zuberbühler2000b; Seyfarth & Cheney, Reference Seyfarth and Cheney2003, Reference Seyfarth and Cheney2010; Hobaiter & Byrne, Reference Hobaiter and Byrne2014).

In this pursuit of the semantic meaning of animal signals, one feature that several scholars were interested in was the possibility that animal signals might exhibit the same level of arbitrariness typical of human language. Several scholars begun to work on ways of detecting and decoding the entire communicative repertoire of animal species (e.g., the work of Slobodchikoff and colleagues on prairie dogs (Cynomys spp.) summarized in Slobodchikoff, Perla & Verdolin, Reference Slobodchikoff, Perla and Verdolin2009). The initial focus was on vocalizations, in part due to the original success of Seyfarth and Cheney’s work on alarm calls and because of the strongly held belief that to in order to understand the evolution of human language one would first have to understand vocal control and vocal learning (referred to in more detail later in this chapter). Initially, scholars adopting this perspective thought of vocalizations (especially alarm calls) as referential (e.g., Seyfarth et al., Reference Seyfarth, Cheney and Marler1980; Slobodchikoff, Kiriazis, Fischer, & Creef, Reference Slobodchikoff, Kiriazis, Fischer and Creef1991; Zuberbühler, Reference Zuberbühler2000a), but more recently there has been a tendency to refer to primate vocalization as “functionally referential” (see e.g., Evans & Evans, Reference Evans and Evans1999; Slocombe & Zuberbühler, Reference Slocombe and Zuberbühler2005) that is, as signals that do not reflect internal states of animals but rather are provoked by external stimuli and convey information about those stimuli, by functioning like words (see, however, Rendall et al., Reference Rendall, Owren and Ryan2009; Wheeler & Fisher, Reference Wheeler and Fischer2012 for criticisms of this concept). Notwithstanding the level of referentiality of animal signals, the logic of this approach invokes that a certain amount of cognition is necessary for the decoding of communicative signals. This approach also often tends to start from human language as a model and the transfer of information between animals is often presented as the key motivation for animal communication.

Several authors have criticized the information perspective on animal communication and the issue of signal honesty (e.g., Dawkins & Krebs, Reference Dawkins, Krebs, Krebs and Davies1978; Owings and Morton, Reference Owings, Morton, Owings, Beecher and Thompson1997, Reference Owings and Morton1998; Stegmann, Reference Stegmann2005; Rendall, Owren, & Ryan, Reference Rendall, Owren and Ryan2009; Owren, Rendall, & Ryan, Reference Owren, Rendall and Ryan2010). One of the main issues is the lack of a precise definition of information in these approaches. Instead of focusing on the information contained in a signal, Dawkins and Krebs (Reference Dawkins, Krebs, Krebs and Davies1978) focus on the sender’s point of view and see communication as a social tool to manipulate the behavior of others. Therefore, the goal of signalers is not to transmit information to receivers. Instead, communication is used to manipulate receivers into performing behavior that benefits the sender. Using the terminology of Owren et al. (Reference Rendall, Owren and Ryan2009), the goal of signalers is to influence recipients. Dawkins and Krebs (Reference Dawkins, Krebs, Krebs and Davies1978) also highlight that signals in cooperative contexts are usually less conspicuous than competitive signals. Because cooperative signals directly benefit receivers, receivers benefit from detecting them right away. In contrast, competitive signals such as threat displays are often times more salient. Krebs and Dawkins (1984) posit that one way to tease apart what led to the development of a signal consists in focusing on whether the signal is amplified, loud, and redundant (probably a competitive origin) or rather reduced (probably a cooperative origin). As they claim, “The evolution of cooperative signaling should lead not to loud, exaggerated, repetitive, conspicuous signals, but to cost-minimizing conspiratorial whispers.” (Krebs & Dawkins, 1984, p. 319). Later in this chapter, we will discuss how this relates to the specific ways of acquiring communicative signals (in particular, gestural ones) recently documented in great apes.

One of the critical points of contention between the information vs. the manipulation perspective is the importance of recipients’ benefits in the occurrence of communication. While the information perspective mostly focuses on what the recipient might gain from properly interpreting what a signal conveys or predicts, the manipulation perspective focuses mostly on the benefits for the signaler and does not quite account for what would lead recipients to invariantly respond to a manipulative signal that benefits only the signaler. Indeed, it would remain unexplained why selection would only work on signalers so that they could produce signals that manipulate recipients but would not operate on recipients themselves, leading them to stop responding to such signals. As noted by Searcy and Nowicki (Reference Searcy and Nowicki2005, p. 8), “If there is, on average, no information of benefit to the receiver in a signal, then receivers should evolve to ignore that signal. If receivers ignore the signal, then signalling no longer has any benefit to the signaller, and the whole communication system should disappear.” Along the same lines, Rossano (Reference Rossano2018) emphasized receivers’ motivation to respond to communicative signals without receiving obvious benefit (e.g., humans’ willingness to respond to requests for directions from strangers) as one of the key problems mostly missing from several language evolution theories.

On the other hand, the manipulation perspective criticized the information perspective because it appears to indirectly assume that social interactions, especially among conspecifics, are mostly cooperative in nature, just as in humans. Indeed, a system that facilitates information transmission or extraction would not be beneficial for animals that are actually competing with each other. Given that social life is mostly competitive in nature (e.g., over mates, food, territories) this would suggest that transmitting information should not be the driving force behind communication. Silk, Kaldor, and Boyd (Reference Silk, Kaldor and Boyd2000), however, demonstrated that honest, low-cost signaling can be an evolutionary stable strategy among individuals with conflicting interests if these individuals interact repeatedly, which is clearly the case for social animals that live in groups. It is important to note that the information perspective was developed by scholars studying nonhuman primates and therefore animals with sophisticated cognitive abilities, complex social systems (that entail both meaningful social bonds and yet also clear hierarchies among individuals), and closer phylogenetic relationships to humans. As previously highlighted for ethologists, considering the species that the researchers have mostly worked with empirically often helps to understand some of the underlying assumptions (and biases) of the communication models proposed. They all have one clear issue in common: They attempt to account for animal communication across all species, rather than acknowledging that several aspects of their ecology (e.g., water vs. air, diurnal vs. nocturnal, solitary vs. social living) and physiology (brain size and neuronal composition) are likely to affect how signals are selected, produced, and processed.

A striking example of how different the perspectives on animal communication can be comes from recent work discussing multimodal communication and multimodal signaling in animals. Biologists tend not to consider whether the signal is under voluntary control by the signaler, and actually focus on the recipient’s perspective. Signals can be perceived via any sensory modality including olfaction, taste, and touch. Scholars from this field usually report on multimodal communication in any animal species and have focused heavily on arthropods (see, e.g., Partan & Marler, Reference Partan and Marler1999, Reference Partan and Marler2005; Aquistapace et al., Reference Acquistapace, Aquiloni, Hazlett and Gherardi2002; Uetz, Roberts, & Taylor, Reference Uetz, Roberts and Taylor2009; Higham & Hebets, Reference Higham and Hebets2013). In contrast, psychological studies of multimodal communication are usually confined to model species among mammals (usually rats and nonhuman primates, sometimes dolphins, or dogs), and focus mostly on the signaler, and on visual and auditory signals that are under the voluntary control of the signaler (see, e.g., Tomasello & Zuberbühler, Reference Tomasello, Zuberbühler, Bekoff, Allen and Burghardt2002; Leavens, Russell, & Hopkins, Reference Leavens, Russell and Hopkins2010; Slocombe, Waller, & Liebal, Reference Slocombe, Waller and Liebal2011).

The importance of voluntary control of signal production, the nature and history of the relationship between the individuals communicating, and the existence of social knowledge and memories that can be accessed in selecting signals brings us to proximate mechanisms.

How Do Animals Communicate? (Proximate Explanations)

We have highlighted how the information perspective on animal communication suggests that signal production in at least some animal species might be more flexible than originally anticipated, and that signal interpretation might also be affected by contextual cues such as who is producing the signal, what is the nature of the relationship between the signaler and the receiver, where is this signal produced, etc. Accordingly, research has focused on the proximate factors that might affect signal selection, and signal learning.

Signal Selection

Ever since Darwin’s (Reference Darwin1871) remarks on animal vocalizations as involuntary expressions of emotions or movement, animal signals have long been considered mostly inflexible, caused by highly emotional situations and ultimately tied to the occurrence of specific perceptual stimuli in the environment. Accordingly, animals would have very limited voluntary control over their signaling and at most they could modify intensity and duration to some degree, but not quite when to produce a signal and which signal to produce. Along the same lines, for example, nonhuman primate vocalizations have long been considered to have similar limitations. The general claim has been that nonhuman primate vocalizations are innate and mostly inflexible, in that primates can partly control intensity and cannot learn new ones. Yet, recent evidence suggests they might have some control over when to produce vocalizations, and some scholars even claim that they do in fact learn to produce novel vocalizations (see Zuberbühler, Reference Zuberbühler2000a; Seyfarth & Cheney, Reference Seyfarth and Cheney2003; Crockford, Wittig, Mundry, & Zuberbühler, Reference Crockford, Wittig, Mundry and Zuberbühler2012; Schel, Townsend, Machanda, Zuberbühler, & Slocombe, Reference Schel, Townsend, Machanda, Zuberbühler and Slocombe2013; Watson et al., Reference Watson, Townsend, Schel, Wilke, Wallace, Cheng, West and Slocombe2015; Lameira, Reference Lameira2017).

On the other hand, the claim that their gestural communication is flexible and under full intentional control and, at least in part it, appears to be learned has been less controversial (Call & Tomasello, Reference Call and Tomasello2007; Schneider, Call, & Liebal, Reference Schneider, Call and Liebal2012; Halina, Rossano, & Tomasello, Reference Halina, Rossano and Tomasello2013; Byrne et al., Reference Byrne, Cartmill, Genty, Graham, Hobaiter and Tanner2017). If this is the case, then it is possible to investigate which criteria primates might rely on to decide which gesture type to use and when. Note here that contrary to the standard use of the term “gesture” in humans, which usually refers only to visible behavior (see Kendon, Reference Kendon2004), when focusing on nonhuman primates, scholars tend to include under this term not only visual signals, but also tactile and auditory signals, such as touching another interactional participant’s body or making noise by hitting the ground (see Call & Tomasello, Reference Call and Tomasello2007). Accordingly, selection of which gestural signal to use could be based on modality, and indeed some recent studies on gestural sequences in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have shown that tactile gestures often precede visual gestures when combined in a sequence (Liebal, Call, & Tomasello, 2004; Hobaiter & Byrne, Reference Hobaiter and Byrne2011a; Rossano, Reference Rossano and Hagoort2019). Yet exceptions exist and can be accounted for by considering the location of the signaler at the time the signal is produced. Indeed, touching an interactional partner becomes impossible if one is physically too far away. If this is the case, then an auditory signal might be produced first, or a visual signal if the recipient is already looking at the signaler.

Interestingly, humans would likely begin an interactional exchange with a vocalization (e.g., calling someone’s name or producing a greeting) or by using a visual signal (e.g., a greeting hand) and physical contact seems to be rather undesired. But humans also systematically rely on what has been called “attention getters” (Liebal et al., Reference Liebal, Call and Tomasello2004a) and on an expectation that a recipient would orient toward a speaker when summoned. Experimental studies on chimpanzees show the opposite pattern. While it has been shown that chimpanzees adapt their communicative behavior to the attentional states of a human recipient (Leavens, Hostetter, Wesley, & Hopkins, Reference Leavens, Hostetter, Wesley and Hopkins2004), if the recipient is not looking at the signaler and the signaler is allowed to move, a chimpanzee is more likely to move around the signaler and place itself in front of the recipient, rather than resorting to an auditory signal to get the interactional partner to turn (Liebal, Call, Tomasello, & Pika, Reference Liebal, Call, Tomasello and Pika2004b). This could account for why tactile gestures are preferred as a way of interacting with a partner: They can be perceived without requiring monitoring of, or adapting to, the recipient gaze direction and simultaneously act as attention getters.

Another interesting aspect of signal sequences concerns what happens when a first signal fails (see e.g., Hobaiter & Byrne, Reference Hobaiter and Byrne2011a on serial gesturing). In a study on interactions between mother–infant bonobos, for example, Rossano (Reference Rossano and Hagoort2019) showed that repeating the same gesture vs. using a new one is not a random decision. If the mother does not respond, infants tend to produce the same gesture, whereas if the mother responds but not in a way that addresses what the infant was trying to elicit, then the infant will produce a different gesture with a similar meaning. This might be equivalent to humans using different expressions to ask a friend for a favor. Moreover, if the same gesture fails to elicit a response multiple times, an infant may resort to producing a different gesture that is more uniquely associated with the action being solicited (e.g., a carry) than the previous one. One could think of the problem here as analogous to the issue of signal ambiguity previously discussed.

This ordering of gestures raises the question of whether there is a possible ranking to them. That is, certain forms may be more effective than others (and their efficacy may change over time), they may convey different interactional nuances (e.g., a response is more or less urgent), or their deployment may have to do with their ontogenetic origins (e.g., the gesture acquired most recently may be the first one to be deployed; see section on learning). Indeed, there is some evidence suggesting that when more than one gestural signal would be available for a chimpanzee to elicit the same type of response, they tend to use more frequently the one that has been more effective in obtaining the desired outcome (see Hobaiter & Byrne, Reference Hobaiter and Byrne2011b, Reference Hobaiter and Byrne2014).

This research suggests that primates might have a general sense of signal effectiveness that becomes a property of the signal and leads to pruning of the gestural repertoire so much so that individuals would stop using some gestures entirely (see Byrne et al., Reference Byrne, Cartmill, Genty, Graham, Hobaiter and Tanner2017). However, more recent work (Kaufhold & Rossano, Reference Kaufhold and Rossano2020) has also shown that signal selection might be affected by the relational history between two individuals, specifically by how an action had played out the most recent time the two animals had interacted (e.g., a food request signal is affected by the previous outcome of a similar request to the same individual). This would suggest that at least some animal species might have a sort of bookkeeping that is more than just a vague emotional bookkeeping (see e.g., Aureli & Schaffner, Reference Aureli and Schaffner2002; Schino & Aureli, Reference Schino and Aureli2009; Crockford et al., Reference Crockford, Wittig, Langergraber, Ziegler and Zuberbühler2013) through which primates remember just the valence of recent encounters with some individuals (e.g., if they were content afterwards or frustrated) but not quite the details of what happened. Rather, these memories might be more specific than currently believed and might include the processing of other contextual cues present at the time a signal was deployed (e.g., the direction of the recipient’s attention, the position of the resource they are trying to obtain, the presence of other group members nearby).

It is therefore important to consider what might be properties of the signal and what might be properties of the context of use and the role that these might play in facilitating or hindering the learning of new signals, especially through development.

Signal Acquisition

According to Seyfarth and Cheney (Reference Seyfarth and Cheney2017), when considering a signal, some of its properties become particularly important toward its optimal acquisition and deployment:
  1. 1 Its informative value (i.e., how clearly it predicts a specific individual or situation)

  2. 2 Its referential specificity (i.e., the breadth of stimuli that would elicit that signal)

  3. 3 The signal specificity (i.e., how distinguishable it is from other signals in the repertoire).

All of the above matters, not just in terms of signal effectiveness, as previously discussed, but also in terms of how easy it might be for an animal to acquire a signal. While some signals satisfy all three features, others satisfy only some of them. In the former case, if all three apply, then the signal is clear and the recipient can easily process it and act accordingly. In the latter case, it is possible that the signal is ambiguous to some degree, and this requires some contextual processing from the recipient. Seyfarth and Cheney (Reference Seyfarth and Cheney2017) provide the example of a baboon (Papio spp.) grunt that is highly nonspecific and is used in a variety of contexts (including as a threat). Yet, if produced after a fight by the aggressor toward the opponent, the grunt can be interpreted as a reconciliatory grunt and usually leads the victim to tolerate the aggressor’s approach or its proximity. In other words, for at least some animal species, signals do not occur in a social vacuum but rather are produced by individuals that have some history affecting not only which signal is produced but also how it is interpreted.

While this is very likely the case for primates, one might wonder to what degree communicative signals in other animal species require this amount of cognitive processing, and to what degree this is learned, rather than an invariant biological predisposition. Communication among invertebrates, for example, appears to be highly ritualized. For example, Karl von Frisch (Reference von Frisch1967) provided detailed documentation of how bees (Apis mellifera) “dance” to indicate the position of food resources to other members of the hive and how this behavior is structured. Peacock spiders (Maratus volans) produce elaborate mating display dances (Girard, Kasumovic, & Elias, Reference Girard, Kasumovic and Elias2011) and so do several other vertebrate animals, such as the Anna’s hummingbirds (Calypte anna), that produce a flying dive while singing (Clark, Reference Clark2009). Courtship rituals often consist of a set of discrete actions that follow a fixed sequence, at times combined with additional signals produced through several modalities over which the animal might have very limited control (see, for example, the coloring and olfactory signals produced by male three-spined sticklebacks (Gasterosteus aculeatus; McLennan, Reference McLennan2003) or the sexual swelling of chimpanzees (Pan troglodytes; e.g., Wallis, Reference Wallis1992)). Importantly, all these signals are shared by all individuals of one species and produced under specific circumstances, independently of learning through the observation of conspecifics.

While some of these signals have evolved specifically for the activity they are currently deployed in, and are the consequence of physiological changes in an animal’s body (e.g., hormonal changes), we know that a large part of animal communicative behavior is actually derived from behaviors and movements that did not have originally any communicative function. This phenomenon, called phylogenetic ritualization, has been extensively documented by ethologists such as Huxley (Reference Huxley1914), Tinbergen (Reference Tinbergen1952), and Lorenz (Reference Lorenz1966). Huxley noted that some animal movements appeared to lose their original function through evolution and ended up being used as signals. Moreover, Lorenz (Reference Lorenz1966) noted that these ritualized movements appear more stereotyped, that is exaggerated, than the movements they had originated from. The ultimate benefit of this stereotypy is the minimization of ambiguity and facilitating recognition of the communicative signal, just as previously highlighted while discussing the concept of “typical intensity” by Morris (Reference Morris1957). According to Lorenz, the movements that have undergone ritualization have done so for two main reasons: (1) canalizing aggression (e.g., dominance displays often include behavioral aspects of fights but without actually damaging the interactional partner); and (2) forming bonds between two or more individuals (e.g., through greeting rituals or via courtship). In other words, the main functions of ritualization are to facilitate relationships among conspecifics and to minimize the escalation of physical conflict. At times, though, the original behavior served a very different function and ended up being borrowed from other contexts and modified to ultimately achieve a communicative function (for example, some courtship movements in birds appear to include what are usually foraging behaviors, see the principle of derived activities, Tinbergen, Reference Tinbergen1952).

If we assume phylogenetic ritualization to be the main mechanism leading to communicative signal formation, then repertoires of each species should be highly uniform and species-specific signals should be used even if individuals never had contact with another conspecific. Yet, in humans, different communities appear to be using different communicative signals (both in terms of vocalizations and in terms of gestural behavior that appear to be language and culture specific). This suggests that at least to some degree, some significant learning (mostly through imitation) has to occur through human ontogeny, both in terms of vocal learning and in terms of gestural learning. This begs the question whether something similar occurs in other animal species.

First, we will begin with the case of gestural learning. In great apes there is an open debate about the likelihood that most of their gestures are innate or learned. There are three main hypotheses on the table (see Liebal, Schneider & Errson-Lembeck, Reference Liebal, Schneider and Errson-Lembeck2019 for a recent review):
  1. 1. Biological inheritance

  2. 2. Ontogenetic ritualization

  3. 3. Cultural learning

Scholars who support the biological inheritance hypothesis suggest that the gestural repertoire of great apes is genetically predetermined and its origin can be entirely accounted for by phylogenetic ritualization (Genty, Breuer, Hobaiter, & Byrne, Reference Genty, Breuer, Hobaiter and Byrne2009; Hobaiter & Byrne, Reference Hobaiter and Byrne2011b; Byrne et al., Reference Byrne, Cartmill, Genty, Graham, Hobaiter and Tanner2017; Graham et al., Reference Byrne, Cartmill, Genty, Graham, Hobaiter and Tanner2017), while those who support the ontogenetic ritualization hypothesis posit that gestures are progressively ritualized within an individual’s lifetime through repeated dyadic interactions and individual repertoires may vary (Tomasello, Call, Nagell, Olguin, & Carpenter, Reference Tomasello, Call, Nagell, Olguin and Carpenter1994; Tomasello et al., Reference Tomasello, Call, Warren, Frost, Carpenter and Nagell1997; Halina et al., Reference Halina, Rossano and Tomasello2013). We may think of this process as something analogous to conventionalization, where individuals end up producing shortened versions of the original behavior because the recipient can anticipatorily recognize what they are trying to achieve. A third hypothesis, the cultural learning hypothesis, suggests that gestures are acquired by imitating those of others in the group (Russon & Galdikas, Reference Russon and Galdikas1993, Reference Russon and Galdikas1995; Tanner, Patterson, & Byrne, Reference Tanner, Patterson and Byrne2006); however, there is no clear empirical support for this claim given the poor imitative skills of great apes (see Tennie, Call, & Tomasello, Reference Tennie, Call and Tomasello2006).

It is oftentimes claimed that the entire gestural repertoire can be explained by a single mechanism. More realistically, a large part of the repertoire is likely biologically predetermined and originates from phylogenetic ritualization, while some other gestures will be learned via social interaction (see Bard et al., Reference Bard, Dunbar, Maguire‐Herring, Veira, Hayes and McDonald2014 for a similar claim on gesture acquisition). Noticeably, all hypotheses emphasize the importance of social interaction for gesture acquisition. For the cultural imitation hypothesis, observation of others interacting is clearly critical. For the ontogenetic ritualization hypothesis, the ritualization of the gesture necessarily occurs while interacting with a cooperative partner that reliably responds to the actions of the signaler. Even supporters of the biological inheritance hypotheses talk about pruning of gestures via testing their effectiveness in social interaction. So, at least as far as great apes are concerned, signal learning does occur through development and their gestural repertoire is not entirely biologically fixed.

A second domain of particular relevance for those interested in language evolution and what makes human speech possible is vocal learning. Vocal learning is usually defined as “the ability to acquire novel vocalizations or modify existing ones on the basis of auditory experience” (see e.g., Lattenkamp & Vernes, Reference Lattenkamp and Vernes2018, p. 209). While many vocalizations are innate and do not depend on experience, others appear to be learned and the infrastructure that allows for this type of learning is of particular interest because it seems relatively rare. A useful framework put forward by Janik and Slater (Reference Janik and Slater2000) distinguishes between:
  1. 1. Comprehension learning

  2. 2. Vocal usage learning

  3. 3. Vocal production learning.

Comprehension learning occurs when an individual can learn to associate a vocalization to an action or outcome (e.g., a dog learning to follow a vocal command). Vocal usage learning occurs when an individual can learn to produce an innate vocalization in a novel context (e.g., a vervet monkey learning to associate a vocalization to a predator). Finally, vocal production learning occurs when an individual’s vocalizations are modified as a result of social interaction with other individuals (e.g., a parrot learning to reproduce human words). Comprehension learning and, to some degree, vocal-usage learning are quite widespread in the animal kingdom due to animals’ abilities to learn through associative learning (Pearce & Bouton, Reference Pearce and Bouton2001). Yet vocal production learning is surprisingly rare, and the classical list of species that can do vocal production learning includes only a few bird orders (i.e., songbirds, parrots, hummingbirds) and some mammals (i.e., humans, elephants, bats, pinnipeds, some cetaceans). These species can produce novel vocalizations through imitation, thanks to a direct connection between the forebrain and phonatory muscles such as the larynx in mammals or syrinx in birds (see Martins & Boeckx, Reference Martins and Boeckx2020). Given the evolutionary distance between the species above and the fact that other closely related species appear to be incapable of vocal learning, the claim is that vocal learning is the product of convergent evolution.

Recent work, however, has begun to challenge a simple dichotomy between species that vocally learn and species that cannot. As such, to better understand the vocal learner phenotype, there have been suggestions to conceive of vocal-learning abilities more as a continuum (see Petkov & Jarvis, Reference Petkov and Jarvis2012), in which some other species can be placed. For example, some nonhuman primate species (e.g., orangutans, Pongo spp., but possibly also chimpanzees, see e.g., Crockford et al., Reference Crockford, Herbinger, Vigilant and Boesch2004; Lameira, Reference Lameira2017) and mice (Arriaga, Zhou, & Jarvis, Reference Arriaga, Zhou and Jarvis2012; but see Hammerschmidt et al., Reference Hammerschmidt, Reisinger, Westekemper, Ehrenreich, Strenzke and Fischer2012 for an opposite claim) have the ability to learn new vocalizations, not necessarily through imitation but rather through some form of social feedback, despite missing some physiological features usually claimed to be key for phonation (e.g., the position of the larynx). Another process might be the improvisation of sounds leading to novel vocalizations, as shown in Bengalese finches (Lonchura striata; Takahasi & Okanoya, Reference Takahasi and Okanoya2010). Along similar lines, Wirthlin and colleagues (Reference Wirthlin, Chang, Knörnschild and Krubitzer2019) have proposed that vocal learning is a multicomponent behavioral phenotype comprising distinct but interconnected modules, and they identify three in particular: vocal coordination (ability to flexibly modify the temporal production of vocal output, e.g., warbling antbirds, Hypocnemis spp.), vocal production variability (ability to dynamically learn new vocalizations throughout development, e.g., common marmoset, Callithrix jacchus), and vocal versatility (repertoire size versus degree to which it can be modified with experience, e.g., Egyptian fruit bat, Rousettus aegyptiacus).

The truth is that we currently lack comparative data on many taxa that would allow us to properly assess how widespread vocal learning abilities really are. Indeed, as shown by Lattenkamp and Vernes (Reference Lattenkamp and Vernes2018), 84 percent of studies published on vocal learning in the last twenty-five years have focused on birds, with about half of them focused on zebra finches (Taeniopygia guttata) as a model animal, and only 8 percent have focused on bats, pinnipeds, cetaceans, and elephants. During the same time period, only 4 percent of studies on vocal learning have focused on nonhuman primates. Luckily, more work on under-investigated taxa is currently underway and new theoretical frameworks are broadening the scope of scholars’ investigations on vocal learning.

New Directions and Open Questions

In what follows we would like to outline some of the new research directions within the field of animal communication:
  • Compositionality and multimodality: Can animals combine signals to produce new meanings? In 1960, the linguist Charles Hockett (Reference Hockett1960) presented a list of thirteen design features of language, and argued that most of these features were likely shared with nonhuman animals. Two of the features that he claimed to be likely unique to human communications were “productivity” and “duality of patterning.” Productivity refers to the ability of conveying new meanings and producing new utterances by recombining signals/words. This enables speakers to produce a sentence that has never been uttered before and yet can be understood by the recipient because of the combinatorial features of human languages called syntax. Duality of patterning on the other hand refers to the ability to rely on combinations of meaningless units (e.g., phonemes) to produce meaningful ones (e.g., words). In recent years, several scholars have looked for traces of these two features in other animal communications, in particular in birds’ and primates’ vocalizations. The term that has been used to refer at different times to either of those abilities is compositionality. Notwithstanding growing evidence of some species ability to combine calls (see e.g., putty nosed monkey (Cercopithecus nictitans), Arnold & Zuberbühler, Reference Arnold and Zuberbühler2012; Campbell’s monkey (Cercopithecus campbelli), Ouattara, Lemasson, & Zuberbühler, Reference Ouattara, Lemasson and Zuberbühler2009; southern pied babbler (Turdoides bicolor), Engesser, Ridley, & Townsend, Reference Engesser, Ridley and Townsend2016; Japanese great tit (Parus minor), Suzuki, Wheatcroft, & Griesser, Reference Suzuki, Wheatcroft and Griesser2016) it is still unclear to what degree the combinatorial abilities of other animals resemble human syntactic abilities (see debate between Bolhuis, Beckers, Huybregts, Berwick, & Everaert, Reference Bolhuis, Beckers, Huybregts, Berwick and Everaert2018; Townsend, Engesser, Stoll, Zuberbühler, & Bickel, Reference Townsend, Engesser, Stoll, Zuberbühler and Bickel2018). In an analogous fashion, the debate around animals’ ability to produce complex meaning through signal combination has been extended to signals produced via different modalities (multimodality): Can animals combine, for example, facial expressions, postures, vocalizations and gestures to produce novel meaning? And is the combination of signals meant to convey novel meaning or is it rather a redundant signal aimed at facilitating perception by the recipient? See Fröhlich, Sievers, Townsend, Gruber, and van Schaik (Reference Fröhlich, Sievers, Townsend, Gruber and Schaik2019) for a recent review of what we know about multimodal signaling in non-human primates.

  • Turn-taking. How are communicators alternating signals while interacting with each other? Is their timing carefully calibrated and are there different types of turn-taking? Cooperative turn-taking is a key hallmark of human communication (see Sacks, Schegloff, & Jefferson, Reference Sacks, Schegloff and Jefferson1974) and several studies have investigated both the structure and timing of conversational turn-taking and to what degree there is cultural variability (see e.g., Stivers et al., Reference Stivers, Enfield, Brown, Englert, Hayashi, Heinemann and Levinson2009; Rossano, Reference Rossano and Hagoort2019). The speed at which humans exchange turns at talk raises interesting questions concerning the cognitive processing power necessary to sustain such a system (see e.g., Garrod & Pickering, Reference Garrod and Pickering2004; Christiansen & Chater, Reference Christiansen and Chater2016; Levinson, Reference Levinson2016). However, recent work on turn-taking and the timing of the gestural communications of chimpanzees and bonobos (see e.g., Rossano, Reference Halina, Rossano and Tomasello2013; Fröhlich et al., Reference Fröhlich, Kuchenbuch, Müller, Fruth, Furuichi, Wittig and Pika2016) has shown strong similarities to what is currently known about humans. More work has been done both on turn-taking in other animal species (e.g., European starlings (Sturnus vulgaris), Henry, Craig, Lemasson, & Hausberger, Reference Henry, Craig, Lemasson, Hausberger, Holler, Casillas and Levinson2016; meerkats (Suricata suricatta), Demartsev, Strandberg-Peshkin, Ruffner, & Manser, Reference Demartsev, Strandburg-Peshkin, Ruffner and Manser2018) and on the development through ontogeny of turn-taking abilities in non-human primates (see e.g., Lemasson et al., Reference Lemasson, Glas, Barbu, Lacroix, Guilloux, Remeuf and Koda2011; Chow, Mitchell, & Miller, Reference Chow, Mitchell and Miller2015; Takahashi, Fenley, & Ghazanfar, Reference Takahashi, Fenley and Ghazanfar2016). Recent work is also attempting to debate similarities and differences between human conversational turn-taking and the gestural and vocal turn-taking documented in other species (see, e.g., Pika, Wilkinson, Kendrick, & Vernes, Reference Pika, Wilkinson, Kendrick and Vernes2018; Rossano, Reference Rossano2018).

  • Acquisition and Development. Are there critical periods for the acquisition of a communicative repertoire? How important is scaffolding and social feedback compared to imitation? Research on animal communication suffers from the difficulty of continuously documenting the daily communicative behavior of the animals under investigation. This is especially problematic if one is interested in the ontogenetic changes and how signals are acquired. Indeed, while we have been able to document the development of communicative abilities in several bird species or domesticated animals (e.g., canids) because of the ease of observing them in laboratories or at home (and thanks to the early work of ethologists), this task is not quite as simple for larger mammals that live in complex wild environments. While we might think of zoos and aquariums as places where the communicative development of most animal species can easily be observed and studied, it is important to remember that these are not natural environments that allow animals to free-range and be exposed to the same challenges and stimulations of their natural ecologies. As such, more work is needed in order to fully understand the importance of social interactions and parental communicative scaffolding in the shaping of animal signals (see for example recent work on young wild chimpanzees by Fröhlich and colleagues, Reference Fröhlich, Müller, Zeiträg, Wittig and Pika2017). As mentioned earlier in this chapter, there is a growing consensus pointing to the crucial importance of social interactions and social environments in the development of communicative repertoires, at least in animals that engage in social learning. The novel technologies that are improving our ability to track wild animals’ behavior in their natural environment (see e.g., Kays, Crofoot, Jetz, & Wikelski, Reference Kays, Crofoot, Jetz and Wikelski2015) will likely revolutionize our understanding of the importance of social shaping and social interaction in the development of communicative signals in non-human animals.

  • Flexibility and Memory. How is signal deployment affected by contextual features and by the ability of animals to keep track of the details of prior interactions? As previously mentioned, it is debated to what degree different animal species have flexible control over the production of communicative signals. This question can be further refined to the point of investigating each species’ degree of flexibility in different modalities. For example, great apes are claimed to have better control of their gestural communication compared to their vocal signals. Besides being able to control when to produce a signal and with which intensity, one might consider whether its production is strongly associated with specific contexts or rather tailored to specific recipients. Some recent studies have made the case that at least great apes can design their communications in relation to specific recipients, both gesturally and vocally (see e.g., Cartmill & Byrne, Reference Cartmill and Byrne2007; Crockford et al., Reference Crockford, Wittig, Mundry and Zuberbühler2012). Yet it remains unclear to what degree prior experiences, either in the same context or with the same recipient, are likely going to affect signal selection. This problem is usually associated with the general question of reciprocity and it is often believed to require a fair amount of memory. Recent work on reciprocity in food sharing in capuchins and chimpanzees has shown that they can keep track of another partner’s recent attitude toward cooperating and sharing, through what has been called attitudinal reciprocity (see de Waal, Reference de Waal2000; Brosnan & de Waal, Reference Brosnan and De Waal2002). Extending this ability beyond the most recent interaction and to longer time spans, other scholars have talked about emotional bookkeeping (see e.g., Aureli & Schaffner, Reference Aureli and Schaffner2002; Schino & Aureli, Reference Schino and Aureli2010; Crockford et al., Reference Crockford, Wittig, Langergraber, Ziegler and Zuberbühler2013). In both cases, the tracking is mostly happening on an emotional level, that is, the animal remembers the positive or negative valence of recent encounters with specific individuals but not the exact details of those interactions. Further empirical studies will have to assess to what degree animal memories are emotionally mediated and which role these memories play in their selection of communicative signals.

  • The issue of one model for all species (but one). Is it helpful to think of animal communication in terms of a few principles that apply to all animal species? Or should we think of a continuum and develop evolutionary models of communications in which animals such as primates are granted some more cognitive abilities and communicative flexibility than for example insects? Space does not allow a review of all papers and books on animal communication that purposefully exclude humans (Homo sapiens) from the species whose communicative behavior should be accounted for under animal communication. Indeed, humans are regularly excluded from animal communication models, and editors and reviewers from biological journals often invite authors investigating animal communication to remove any reference to research on humans. While anthropomorphizing animals is most certainly a mistake that we should carefully avoid, it is equally problematic to remove humans from the animal kingdom. One of the main reasons to exclude humans from the models comes from a desire to account for animal communicative behavior without having to include any reference to their cognitive abilities. Our suggestion is to be more inclusive and, as such, to at least consider as a possibility the fact that the communicative behavior of a chimpanzee (Pan troglodytes) might have more in common with the behavior of a human being than to the behavior of a fruit fly (Drosophila melanogaster). Future research should ideally address the resistance of several scholars to accept the use of terminology referring to the cognitive abilities of specific animals, not by imposing it but simply by showing how the inclusion of these variables provides a significantly enhanced predictive power and better captures the nuances of the communicative system of each species.

Conclusions

Communication is commonplace in the animal kingdom. It can be observed in a wide range of relationships and expressed through different modalities with varying timescales. It ranges across varying degrees of flexibility and cognitive effort for both senders and receivers. This chapter can only provide a glimpse into the myriad of communication systems that can be found across different animal species. One shared feature of all communication systems is that signals are, on average, beneficial (i.e., adaptive) for senders and receivers. This can be the case in cooperative relationships between kin, conspecifics, and heterospecifics. However, communication can also arise within competitive relationships. Here, communication can help to avoid negative outcomes, such as resource loss, injury or even death from conflicts with rivals or potential predators. We reviewed some of the early scientific studies of animal signals by ethologists such as Konrad Lorenz and Nikolaas Tinbergen. These early investigations into animals’ communication came mainly from a phylogenetic perspective and focused on the behaviors that communication signals derived from, for example in the context of courtship rituals (see derived activities and phylogenetic ritualization). In general, animals use personal information (perception and direct interaction with the environment) and social information (observing other organisms) to guide their behavior. Social information can comprise both cues and signals. Signals develop when the transmission of social information is on average good for both the sender and recipient’s fitness. Signals can be divided into self-reporting (e.g., warning coloration) and other-reporting signals (e.g., alarm calls) and are usually designed according to recipients’ perception and cognitive abilities to reduce the effort that is needed to receive them and comprehend them. Consequently, signals can be multimodal and include redundancy, for example via repetition. Communication systems can be vulnerable to deception when a conspecific or heterospecific can exploit them to their own benefits. The danger of exploitation through deception can be mitigated through mechanisms such as costly or honest signals, that is, signals that are too costly to be easily faked. Communication systems are also susceptible to eavesdropping, which occurs when signals are picked up by third parties that are not the intended recipients, which can result in neutral, negative, or positive consequences for the signaler. We further sketched the ongoing debate between the information perspective and manipulation perspective of animal communication. While the former assumes that signals are designed to pass information from a sender to a receiver for their benefit, the latter assumes that signalers main goal is the manipulation of a recipient’s behavior to the signalers benefit. In our section on proximate aspects of animal communication, we both addressed aspects of signal selection, that is whether and how animals produce signals under specific circumstances, and mechanisms concerning how animals acquire their signal repertoire. While in the past animal communication has mainly been regarded as involuntary responses to external stimuli, recent research with primates revealed a high degree of flexibility, especially for gestural communication. Great apes have been shown to adjust their gestural signaling according to the previous interactions, attentional states, and reactions of recipients. In contrast, certain animal signals are highly inflexible, such as the warning colorations of poisonous frogs. This corresponds to our discussion of different mechanisms that lead to the acquisition of a signal repertoire in animals. Signals can be acquired through ultimate mechanisms. The warning coloration in poisonous frogs is acquired through biological inheritance, for example, and courtship displays in birds through phylogenetic ritualization. However, many animals also acquire signals within their individual lifespan through proximate mechanisms such as ontogenetic ritualization and cultural learning. While the specific social-learning mechanisms for signals are debated, the existence of variation of signals within species is evidence for the presence of ontogenetic acquisition mechanisms across many species. Vocal learning is one of the ontogenetic mechanisms that has received much attention in recent years and can be divided into comprehension learning, vocal usage learning, and vocal production learning according to the framework provided by Janik and Slater (Reference Janik and Slater2000). While vocal learning is most prominent in humans and birds, it developed separately in a range of distantly related species through convergent evolution. Given that work on vocal-learning abilities has been conducted on only a few species and at very different levels of granularity, we likely do not yet know both the full extent of flexibility of this ability and the ecological pressures that led to its development. More research on signal selection and signal acquisition (in particular on social learning) is likely to provide key insights on the processes that led to language evolution in humans. Moreover, we are likely going to see considerable new research addressing issues such as compositionality and multimodality, how animals’ turn-taking compares to human conversational turn-taking, and to what degree animals’ cognitive abilities (e.g., their memories of prior interactions) affect their communications. Ultimately, future research will better serve our scientific understanding of the evolution of animal communication by expanding the documentation of the communicative system to a wider range of species (beyond model species of birds and mammals). Finally, rather than focusing on a one-model-fits-all approach with very limited explanatory power, we should consider placing communicative systems on a continuum (or several ones, if we want to break communicative systems down in terms of specific mechanisms or features such as learnability, flexibility, modalities, etc.). Ideally, this continuum should be inclusive of all animal species and as such, it should not exclude humans (Homo sapiens).

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