The function and consequences of fluorescence in tetrapods.

Fluorescence, the optical phenomenon whereby short-wavelength light is absorbed and emitted at longer wavelengths, has been widely described in aquatic habitats, in both invertebrates and fish. Recent years have seen a stream of articles reporting fluorescence, ranging from frogs, platypus, to even fully terrestrial organisms such as flying squirrels, often explicitly or implicitly linking the presence of fluorescence with sexual selection and communication. However, many of these studies fail to consider the physiological requirements of evolutionary stable signaling systems, the environmental dependence of perception, or the possible adaptive role of fluorescent coloration in a noncommunicative context. More importantly, the idea that fluorescence may simply constitute an indirect by-product of selection on other traits is often not explored. This is especially true for terrestrial systems where environmental light conditions are often not amenable for fluorescent signaling in contrast to, for example, aquatic habitats in which spectral properties of water promote functional roles for fluorescence. Despite the appeal of previously unknown ways in which coloration may drive evolution, the investigation of a putative role of fluorescence in communication must be tempered by a realistic understanding of its limitations. Here, we not only highlight and discuss the key body of literature but also address the potential pitfalls when reporting fluorescence and how to solve them. In addition, we propose exciting different research avenues to advance the field of tetrapod fluorescence.

Not your private tête-à-tête: leveraging the power of higher-order networks to study animal communication.

Animal communication is frequently studied with conventional network representations that link pairs of individuals who interact, for example, through vocalization. However, acoustic signals often have multiple simultaneous receivers, or receivers integrate information from multiple signallers, meaning these interactions are not dyadic. Additionally, non-dyadic social structures often shape an individual's behavioural response to vocal communication. Recently, major advances have been made in the study of these non-dyadic, higher-order networks (e.g. hypergraphs and simplicial complexes). Here, we show how these approaches can provide new insights into vocal communication through three case studies that illustrate how higher-order network models can: (i) alter predictions made about the outcome of vocally coordinated group departures; (ii) generate different patterns of song synchronization from models that only include dyadic interactions; and (iii) inform models of cultural evolution of vocal communication. Together, our examples highlight the potential power of higher-order networks to study animal vocal communication. We then build on our case studies to identify key challenges in applying higher-order network approaches in this context and outline important research questions that these techniques could help answer. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Hidden social complexity behind vocal and acoustic communication in non-avian reptiles.

Social interactions are inevitable in the lives of most animals, since most essential behaviours require interaction with conspecifics, such as mating and competing for resources. Non-avian reptiles are typically viewed as solitary animals that predominantly use their vision and olfaction to communicate with conspecifics. Nevertheless, in recent years, evidence is mounting that some reptiles can produce sounds and have the potential for acoustic communication. Reptiles that can produce sound have an additional communicative channel (in addition to visual/olfactory channels), which could suggest they have a higher communicative complexity, the evolution of which is assumed to be driven by the need of social interactions. Thus, acoustic reptiles may provide an opportunity to unveil the true social complexity of reptiles that are usually thought of as solitary. This review aims to reveal the hidden social interactions behind the use of sounds in non-avian reptiles. Our review suggests that the potential of vocal and acoustic communication and the complexity of social interactions may be underestimated in non-avian reptiles, and that acoustic reptiles may provide a great opportunity to uncover the coevolution between sociality and communication in non-avian reptiles. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

The relative contribution of acoustic signals versus movement cues in group coordination and collective decision-making.

To benefit from group living, individuals need to maintain cohesion and coordinate their activities. Effective communication thus becomes critical, facilitating rapid coordination of behaviours and reducing consensus costs when group members have differing needs and information. In many bird and mammal species, collective decisions rely on acoustic signals in some contexts but on movement cues in others. Yet, to date, there is no clear conceptual framework that predicts when decisions should evolve to be based on acoustic signals versus movement cues. Here, we first review how acoustic signals and movement cues are used for coordinating activities. We then outline how information masking, discrimination ability (Weber's Law) and encoding limitations, as well as trade-offs between these, can identify which types of collective behaviours likely rely on acoustic signals or movement cues. Specifically, our framework proposes that behaviours involving the timing of events or expression of specific actions should rely more on acoustic signals, whereas decisions involving complex choices with multiple options (e.g. direction and destination) should generally use movement cues because sounds are more vulnerable to information masking and Weber's Law effects. We then discuss potential future avenues of enquiry, including multimodal communication and collective decision-making by mixed-species animal groups. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamic'.

Benefits but not the dual functions of submissive signals differ between two Malagasy primates.

Many animals use formalized signals to communicate dominance relationships. In some primates, such as macaques, the function of such signals varies with dominance style. Despotic species produce unidirectional submission signals that have a dual function: in conflict contexts, they signal a willingness to withdraw, whereas in peaceful contexts, they indicate the agreement to subordination. More despotic species produce these calls to a lesser extent than less despotic species. Here, we investigated whether the use of unidirectional submission signals is also related to dominance style in two lemur species and whether signalling subordination stabilizes social relationships at the group level. Ring-tailed lemurs (Lemur catta) exhibit a more despotic dominance hierarchy than Verreaux's sifakas (Propithecus verreauxi). We observed social interactions in 75 dyads of Verreaux's sifakas and 118 dyads of ring-tailed lemurs. Both species used unidirectional submissive calls that have a dual function, potentially suggesting convergent evolution of the function of these signals in independent primate lineages. However, signalling subordination did not stabilize social relationships at the group level in both species. Additionally, subordination occurred more frequently in dyads of the more despotic ring-tailed lemurs than in Verreaux's sifakas, indicating opposite patterns to macaques in the coevolution of social traits with dominance style. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Individual and ecological heterogeneity promote complex communication in social vertebrate group decisions.

To receive the benefits of social living, individuals must make effective group decisions that enable them to achieve behavioural coordination and maintain cohesion. However, heterogeneity in the physical and social environments surrounding group decision-making contexts can increase the level of difficulty social organisms face in making decisions. Groups that live in variable physical environments (high ecological heterogeneity) can experience barriers to information transfer and increased levels of ecological uncertainty. In addition, in groups with large phenotypic variation (high individual heterogeneity), individuals can have substantial conflicts of interest regarding the timing and nature of activities, making it difficult for them to coordinate their behaviours or reach a consensus. In such cases, active communication can increase individuals' abilities to achieve coordination, such as by facilitating the transfer and aggregation of information about the environment or individual behavioural preferences. Here, we review the role of communication in vertebrate group decision-making and its relationship to heterogeneity in the ecological and social environment surrounding group decision-making contexts. We propose that complex communication has evolved to facilitate decision-making in specific socio-ecological contexts, and we provide a framework for studying this topic and testing related hypotheses as part of future research in this area. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Collective signalling is shaped by feedbacks between signaller variation, receiver perception and acoustic environment in a simulated communication network.

Communication takes place within a network of multiple signallers and receivers. Social network analysis provides tools to quantify how an individual's social positioning affects group dynamics and the subsequent biological consequences. However, network analysis is rarely applied to animal communication, likely due to the logistical difficulties of monitoring natural communication networks. We generated a simulated communication network to investigate how variation in individual communication behaviours generates network effects, and how this communication network's structure feeds back to affect future signalling interactions. We simulated competitive acoustic signalling interactions among chorusing individuals and varied several parameters related to communication and chorus size to examine their effects on calling output and social connections. Larger choruses had higher noise levels, and this reduced network density and altered the relationships between individual traits and communication network position. Hearing sensitivity interacted with chorus size to affect both individuals' positions in the network and the acoustic output of the chorus. Physical proximity to competitors influenced signalling, but a distinctive communication network structure emerged when signal active space was limited. Our model raises novel predictions about communication networks that could be tested experimentally and identifies aspects of information processing in complex environments that remain to be investigated. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Multimodal communication and audience directedness in the greeting behaviour of semi-captive African savannah elephants.

Many species communicate by combining signals into multimodal combinations. Elephants live in multi-level societies where individuals regularly separate and reunite. Upon reunion, elephants often engage in elaborate greeting rituals, where they use vocalisations and body acts produced with different body parts and of various sensory modalities (e.g., audible, tactile). However, whether these body acts represent communicative gestures and whether elephants combine vocalisations and gestures during greeting is still unknown. Here we use separation-reunion events to explore the greeting behaviour of semi-captive elephants (Loxodonta africana). We investigate whether elephants use silent-visual, audible, and tactile gestures directing them at their audience based on their state of visual attention and how they combine these gestures with vocalisations during greeting. We show that elephants select gesture modality appropriately according to their audience's visual attention, suggesting evidence of first-order intentional communicative use. We further show that elephants integrate vocalisations and gestures into different combinations and orders. The most frequent combination consists of rumble vocalisations with ear-flapping gestures, used most often between females. By showing that a species evolutionarily distant to our own primate lineage shows sensitivity to their audience's visual attention in their gesturing and combines gestures with vocalisations, our study advances our understanding of the emergence of first-order intentionality and multimodal communication across taxa.

Male proboscis monkey cranionasal size and shape is associated with visual and acoustic signalling.

The large nose adorned by adult male proboscis monkeys is hypothesised to serve as an audiovisual signal of sexual selection. It serves as a visual signal of male quality and social status, and as an acoustic signal, through the expression of loud, low-formant nasalised calls in dense rainforests, where visibility is poor. However, it is unclear how the male proboscis monkey nasal complex, including the internal structure of the nose, plays a role in visual or acoustic signalling. Here, we use cranionasal data to assess whether large noses found in male proboscis monkeys serve visual and/or acoustic signalling functions. Our findings support a visual signalling function for male nasal enlargement through a relatively high degree of nasal aperture sexual size dimorphism, the craniofacial region to which nasal soft tissue attaches. We additionally find nasal aperture size increases beyond dental maturity among male proboscis monkeys, consistent with the visual signalling hypothesis. We show that the cranionasal region has an acoustic signalling role through pronounced nasal cavity sexual shape dimorphism, wherein male nasal cavity shape allows the expression of loud, low-formant nasalised calls. Our findings provide robust support for the male proboscis monkey nasal complex serving both visual and acoustic functions.

Production of sounds by squirrelfish during symbiotic relationships with cleaner wrasses.

Examples of symbiotic relationships often include cleaning mutualisms, typically involving interactions between cleaner fish and other fish, called the clients. While these cleaners can cooperate by removing ectoparasites from their clients, they can also deceive by feeding on client mucus, a behavior usually referred to as "cheating behavior" that often leads to a discernible jolt from the client fish. Despite extensive studies of these interactions, most research has focused on the visual aspects of the communication. In this study, we aimed to explore the role of acoustic communication in the mutualistic relationship between cleaner fishes and nine holocentrid client species across four regions of the Indo-Pacific Ocean: French Polynesia, Guam, Seychelles, and the Philippines. Video cameras coupled with hydrophones were positioned at various locations on reefs housing Holocentridae fish to observe their acoustic behaviors during interactions. Our results indicate that all nine species of holocentrids can use acoustic signals to communicate to cleaner fish their refusal of the symbiotic interaction or their desire to terminate the cooperation. These sounds were predominantly observed during agonistic behavior and seem to support visual cues from the client. This study provides a novel example of acoustic communication during a symbiotic relationship in teleosts. Interestingly, these vocalizations often lacked a distinct pattern or structure. This contrasts with numerous other interspecific communication systems where clear and distinguishable signals are essential. This absence of a clear acoustic pattern may be because they are used in interspecific interactions to support visual behavior with no selective pressure for developing specific calls required in conspecific recognition. The different sound types produced could also be correlated with the severity of the client response. There is a need for further research into the effects of acoustic behaviors on the quality and dynamics of these mutualistic interactions.

Neuroethology: Decoding the waggle dance.

A new study combining high-speed video recordings and computational modeling has revealed an overlooked feature of the famous honeybee waggle dance, yielding the first biologically plausible neural circuit model of how the information transmitted via the waggle dance could be assimilated by the follower bees.

Gestural communication in wild spider monkeys (Ateles geoffroyi).

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy's spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals' gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients' attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

Collective sensing in electric fish.

A number of organisms, including dolphins, bats and electric fish, possess sophisticated active sensory systems that use self-generated signals (for example, acoustic or electrical emissions) to probe the environment1,2. Studies of active sensing in social groups have typically focused on strategies for minimizing interference from conspecific emissions2-4. However, it is well known from engineering that multiple spatially distributed emitters and receivers can greatly enhance environmental sensing (for example, multistatic radar and sonar)5-8. Here we provide evidence from modelling, neural recordings and behavioural experiments that the African weakly electric fish Gnathonemus petersii utilizes the electrical pulses of conspecifics to extend its electrolocation range, discriminate objects and increase information transmission. These results provide evidence for a new, collective mode of active sensing in which individual perception is enhanced by the energy emissions of nearby group members.

Dynamic antennal positioning allows honeybee followers to decode the dance.

The honeybee waggle dance has been widely studied as a communication system, yet we know little about how nestmates assimilate the information needed to navigate toward the signaled resource. They are required to detect the dancer's orientation relative to gravity and duration of the waggle phase and translate this into a flight vector with a direction relative to the sun1 and distance from the hive.2,3 Moreover, they appear capable of doing so from varied, dynamically changing positions around the dancer. Using high-speed, high-resolution video, we have uncovered a previously unremarked correlation between antennal position and the relative body axes of dancer and follower bees. Combined with new information about antennal inputs4,5 and spatial encoding in the insect central complex,6,7 we show how a neural circuit first proposed to underlie path integration could be adapted to decoding the dance and acquiring the signaled information as a flight vector that can be followed to the resource. This provides the first plausible account of how the bee brain could support the interpretation of its dance language.

Importance of the receiver's height for transmission studies in acoustic ecology.

In animal communication, the sound pressure level (SPL) of the acoustic signals has been studied in relation to various biological functions. Previous research reported that senders and receivers benefit from being at elevated positions. However, sometimes, researchers find contradictory results. Using a transmission experiment, we measured SPL of two acoustic stimuli: (i) white noise, and (ii) advertisement calls of the Iberian tree frog (Hyla molleri) at two different heights above ground level (0.05 and 0.75 m) and from six distances (1, 2, 4, 8, 16, and 32 m) from a loudspeaker. Calls of the Iberian tree frog have two spectral peaks centred at the frequencies of ca. 1 and 2 kHz. As expected, SPL decreased with distance, but following a distinct attenuation pattern across height above the ground and frequency. Our findings show that the ground effect may critically alter frequency attenuation and, therefore, signal composition and discrimination at the listener's location, even at low heights above the ground. We suggest that recording devices should be positioned at the same height that natural listeners are usually located in nature, to facilitate the replication and comparison of experiments in the field of acoustic ecology and, also, bioacoustics.

The 'after you' gesture in a bird.

Gestures are ubiquitous in human communication, involving movements of body parts produced for a variety of purposes, such as pointing out objects (deictic gestures) or conveying messages (symbolic gestures)1. While displays of body parts have been described in many animals2, their functional similarity to human gestures has primarily been explored in great apes3,4, with little research attention given to other animal groups. To date, only a few studies have provided evidence for deictic gestures in birds and fish5,6,7, but it is unclear whether non-primate animals can employ symbolic gestures, such as waving to mean 'goodbye', which are, in humans, more cognitively demanding than deictic gestures1. Here, we report that the Japanese tit (Parus minor), a socially monogamous bird, uses wing-fluttering to prompt their mated partner to enter the nest first, and that wing-fluttering functions as a symbolic gesture conveying a specific message ('after you'). Our findings encourage further research on animal gestures, which may help in understanding the evolution of complex communication, including language.

Moss bugs shed light on the evolution of complex bioacoustic systems.

Vibroacoustic signalling is one of the dominant strategies of animal communication, especially in small invertebrates. Among insects, the order Hemiptera displays a staggering diversity of vibroacoustic organs and is renowned for possessing biomechanically complex elastic recoil devices such as tymbals and snapping organs that enable robust vibrational communication. However, our understanding of the evolution of hemipteran elastic recoil devices is hindered by the absence of relevant data in the phylogenetically important group known as moss bugs (Coleorrhyncha), which produce substrate-borne vibrations through an unknown mechanism. In the present work, we reveal the functional morphology of the moss bug vibrational mechanism and study its presence across Coleorrhyncha and in extinct fossilised relatives. We incorporate the anatomical features of the moss bug vibrational mechanism in a phylogeny of Hemiptera, which supports either a sister-group relationship to Heteroptera, or a sister-group relationship with the Auchenorrhyncha. Regardless of topology, we propose that simple abdominal vibration was present at the root of Euhemiptera, and arose 350 million years ago, suggesting that this mode of signalling is among the most ancient in the animal kingdom. Therefore, the most parsimonious explanation for the origins of complex elastic recoil devices is that they represent secondary developments that arose exclusively in the Auchenorrhyncha.

How new communication behaviors evolve: Androgens as modifiers of neuromotor structure and function in foot-flagging frogs.

How diverse animal communication signals have arisen is a question that has fascinated many. Xenopus frogs have been a model system used for three decades to reveal insights into the neuroendocrine mechanisms and evolution of vocal diversity. Due to the ease of studying central nervous system control of the laryngeal muscles in vitro, Xenopus has helped us understand how variation in vocal communication signals between sexes and between species is produced at the molecular, cellular, and systems levels. Yet, it is becoming easier to make similar advances in non-model organisms. In this paper, we summarize our research on a group of frog species that have evolved a novel hind limb signal known as 'foot flagging.' We have previously shown that foot flagging is androgen dependent and that the evolution of foot flagging in multiple unrelated species is accompanied by the evolution of higher androgen hormone sensitivity in the leg muscles. Here, we present new preliminary data that compare patterns of androgen receptor expression and neuronal cell density in the lumbar spinal cord - the neuromotor system that controls the hind limb - between foot-flagging and non-foot-flagging frog species. We then relate our work to prior findings in Xenopus, highlighting which patterns of hormone sensitivity and neuroanatomical structure are shared between the neuromotor systems underlying Xenopus vocalizations and foot-flagging frogs' limb movement and which appear to be species-specific. Overall, we aim to illustrate the power of drawing inspiration from experiments in model organisms, in which the mechanistic details have been worked out, and then applying these ideas to a non-model species to reveal new details, further complexities, and fresh hypotheses.

Ultrafast sound production mechanism in one of the smallest vertebrates.

Motion is the basis of nearly all animal behavior. Evolution has led to some extraordinary specializations of propulsion mechanisms among invertebrates, including the mandibles of the dracula ant and the claw of the pistol shrimp. In contrast, vertebrate skeletal movement is considered to be limited by the speed of muscle, saturating around 250 Hz. Here, we describe the unique propulsion mechanism by which Danionella cerebrum, a miniature cyprinid fish of only 12 mm length, produces high amplitude sounds exceeding 140 dB (re. 1 µPa, at a distance of one body length). Using a combination of high-speed video, micro-computed tomography (micro-CT), RNA profiling, and finite difference simulations, we found that D. cerebrum employ a unique sound production mechanism that involves a drumming cartilage, a specialized rib, and a dedicated muscle adapted for low fatigue. This apparatus accelerates the drumming cartilage at over 2,000 g, shooting it at the swim bladder to generate a rapid, loud pulse. These pulses are chained together to make calls with either bilaterally alternating or unilateral muscle contractions. D. cerebrum use this remarkable mechanism for acoustic communication with conspecifics.

The active space of sperm whale codas: inter-click information for intra-unit communication.

Sperm whales (Physeter macrocephalus) are social mega-predators who form stable matrilineal units that often associate within a larger vocal clan. Clan membership is defined by sharing a repertoire of coda types consisting of specific temporal spacings of multi-pulsed clicks. It has been hypothesized that codas communicate membership across socially segregated sympatric clans, but others propose that codas are primarily used for behavioral coordination and social cohesion within a closely spaced social unit. Here, we test these hypotheses by combining measures of ambient noise levels and coda click source levels with models of sound propagation to estimate the active space of coda communication. Coda clicks were localized off the island of Dominica with a four- or five-element 80 m vertical hydrophone array, allowing us to calculate the median RMS source levels of 1598 clicks from 444 codas to be 161 dB re. 1 µPa (IQR 153-167), placing codas among the most powerful communication sounds in toothed whales. However, together with measured ambient noise levels, these source levels lead to a median active space of coda communication of ∼4 km, reflecting the maximum footprint of a single foraging sperm whale unit. We conclude that while sperm whale codas may contain information about clan affiliation, their moderate active space shows that codas are not used for long range acoustic communication between units and clans, but likely serve to mediate social cohesion and behavioral transitions in intra-unit communication.