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.

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.

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.

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.

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.

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.

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.

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.

On the function of a female-like signal type in the vibrational repertoire of Enchenopa male treehoppers (Hemiptera: Membracidae).

Animals often mimic the behaviours or signals of conspecifics of the opposite sex while courting. We explored the potential functions of a novel female-like signal type in the courtship displays of male Enchenopa treehoppers. In these plant-feeding insects, males produce plant-borne vibrational advertisement signals, to which females respond with their own duetting signals. Males also produce a signal type that resembles the female duetting responses. We experimentally tested whether this signal modifies the behaviour of receivers. First, we tested whether the female-like signal would increase the likelihood of a female response. However, females were as likely to respond to playbacks with or without them. Second, we tested whether the female-like signal would inhibit competing males, but males were as likely to produce displays after playbacks with or without them. Hence, we found no evidence that this signal has an adaptive function, despite its presence in the courtship display, where sexual selection affects signal features. Given these findings, we also explored whether the behavioural and morphological factors of the males were associated with the production of the female-like signal. Males that produced this signal had higher signalling effort (longer and more frequent signals) than males that did not produce it, despite being in worse body condition. Lastly, most males were consistent over time in producing the female-like signal or not. These findings suggest that condition-dependent or motivational factors explain the presence of the female-like signal. Alternatively, this signal might not bear an adaptive function, and it could be a way for males to warm up or practice signalling, or even be a by-product of how signals are transmitted through the plant. We suggest further work that might explain our puzzling finding that a signal in the reproductive context might not have an adaptive function.

Primate socio-ecology shapes the evolution of distinctive facial repertoires.

Primate facial musculature enables a wide variety of movements during bouts of communication, but how these movements contribute to signal construction and repertoire size is unclear. The facial mobility hypothesis suggests that morphological constraints shape the evolution of facial repertoires: species with higher facial mobility will produce larger and more complex repertoires. In contrast, the socio-ecological complexity hypothesis suggests that social needs shape the evolution of facial repertoires: as social complexity increases, so does communicative repertoire size. We tested these two hypotheses by comparing chimpanzees (Pan troglodytes) and gibbons (family Hylobatidae), two distantly related apes who vary in their facial mobility and social organization. While gibbons have higher facial mobility than chimpanzees, chimpanzees live in more complex social groups than gibbons. We compared the morphology and complexity of facial repertoires for both apes using Facial Action Coding Systems designed for chimpanzees and gibbons. Our comparisons were made at the level of individual muscle movements (action units [AUs]) and the level of muscle movement combinations (AU combinations). Our results show that the chimpanzee facial signaling repertoire was larger and more complex than gibbons, consistent with the socio-ecological complexity hypothesis. On average, chimpanzees produced AU combinations consisting of more morphologically distinct AUs than gibbons. Moreover, chimpanzees also produced more morphologically distinct AU combinations than gibbons, even when focusing exclusively on AUs present in both apes. Therefore, our results suggest that socio-ecological factors were more important than anatomical ones to the evolution of facial signaling repertoires in chimpanzees and gibbons. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

GesturalOrigins: A bottom-up framework for establishing systematic gesture data across ape species.

Current methodologies present significant hurdles to understanding patterns in the gestural communication of individuals, populations, and species. To address this issue, we present a bottom-up data collection framework for the study of gesture: GesturalOrigins. By "bottom-up", we mean that we minimise a priori structural choices, allowing researchers to define larger concepts (such as 'gesture types', 'response latencies', or 'gesture sequences') flexibly once coding is complete. Data can easily be re-organised to provide replication of, and comparison with, a wide range of datasets in published and planned analyses. We present packages, templates, and instructions for the complete data collection and coding process. We illustrate the flexibility that our methodological tool offers with worked examples of (great ape) gestural communication, demonstrating differences in the duration of action phases across distinct gesture action types and showing how species variation in the latency to respond to gestural requests may be revealed or masked by methodological choices. While GesturalOrigins is built from an ape-centred perspective, the basic framework can be adapted across a range of species and potentially to other communication systems. By making our gesture coding methods transparent and open access, we hope to enable a more direct comparison of findings across research groups, improve collaborations, and advance the field to tackle some of the long-standing questions in comparative gesture research.

Honey bee colonies change their foraging decisions after in-hive experiences with unsuitable pollen.

Pollen is the protein resource for Apis mellifera and its selection affects colony development and productivity. Honey bee foragers mainly lose their capacity to digest pollen, so we expect that those pollen constituents that can only be evaluated after ingestion will not influence their initial foraging preferences at food sources. We predicted that pollen composition may be evaluated in a delayed manner within the nest, for example, through the effects that the pollen causes on the colony according to its suitability after being used by in-hive bees. To address whether pollen foraging is mediated by in-hive experiences, we conducted dual-choice experiments to test the avoidance of pollen adulterated with amygdalin, a deterrent that causes post-ingestion malaise. In addition, we recorded pollen selection in colonies foraging in the field after being supplied or not with amygdalin-adulterated pollen from one of the dominant flowering plants (Diplotaxis tenuifolia). Dual-choice experiments revealed that foragers did not avoid adulterated pollens at the foraging site; however, they avoided pollen that had been offered adulterated within the nest on the previous days. In field experiments, pollen samples from colonies supplied with amygdalin-adulterated pollen were more diverse than controls, suggesting that pollen foraging was biased towards novel sources. Our findings support the hypothesis that pollen assessment relies on in-hive experiences mediated by pollen that causes post-ingestive malaise.

Coupled information networks drive honeybee (Apis mellifera) collective foraging.

Collective behaviour by eusocial insect colonies is typically achieved through multiple communication networks that produce complex behaviour at the group level but often appear to provide redundant or even competing information. A classic example occurs in honeybee (Apis mellifera) colonies, where both the dance communication system and robust scent-based mechanisms contribute to the allocation of a colony's workforce by regulating the flow of experienced foragers among known food sources. Here we analysed social connectivity patterns during the reactivation of experienced foragers to familiar feeding sites to show that these social information pathways are not simply multiple means to achieve the same end but intersect to play complementary roles in guiding forager behaviour. Using artificial feeding stations, we mimicked a natural scenario in which two forager groups were simultaneously collecting from distinct patches containing different flowering species. We then observed the reactivation of these groups at their familiar feeding sites after interrupting their foraging. Social network analysis revealed that temporarily unemployed individuals interacted more often and for longer with foragers that advertised a familiar versus unfamiliar foraging site. Due to such resource-based assortative mixing, network-based diffusion analysis estimated that reactivation events primarily resulted from interactions among bees that had been trained to the same feeding station and less so from different-feeder interactions. Both scent- and dance-based interactions strongly contributed to reactivation decisions. However, each bout of dance-following had an especially strong effect on a follower's likelihood of reactivation, particularly when dances indicated locations familiar to followers. Our findings illustrate how honeybee foragers can alter their social connectivity in ways that are likely to enhance collective outcomes by enabling foragers to rapidly access up-to-date information about familiar foraging sites. In addition, our results highlight how reliance on multiple communication mechanisms enables social insect workers to utilise flexible information-use strategies that are robust to variation in the availability of social information.

The relationship between body size and stridulatory sound production in loricariid catfishesa).

Sound production capabilities and characteristics in Loricariidae, the largest catfish family, have not been well examined. Sounds produced by three loricariid catfish species, Otocinclus affinis, Pterygoplichthys gibbiceps, and Pterygoplichthys pardalis, were recorded. Each of these species produces pulses via pectoral-fin spine stridulation by rubbing the ridged condyle of the dorsal process of the pectoral-fin spine base against a matching groove-like socket in the pectoral girdle. Light and scanning electron microscopy were used to examine the dorsal process of the pectoral-fin spines of these species. Mean distances between dorsal process ridges of O. affinis, P. gibbiceps, and P. pardalis were 53, 161, and 329 µm, respectively. Stridulation sounds occurred during either abduction (type A) or adduction (type B). O. affinis produced sounds through adduction only and P. pardalis through abduction only, whereas P. gibbiceps often produced pulse trains alternating between abduction and adduction. In these species, dominant frequency was an inverse function of sound duration, fish total length, and inter-ridge distance on the dorsal process of the pectoral-fin spine and sound duration increased with fish total length. While stridulation sounds are used in many behavioral contexts in catfishes, the functional significance of sound production in Loricariidae is currently unknown.

A volatilized pyrethroid insecticide from a mosquito repelling device does not impact honey bee foraging and recruitment.

Because nontarget, beneficials, like insect pollinators, may be exposed unintentionally to insecticides, it is important to evaluate the impact of chemical controls on the behaviors performed by insect pollinators in field trials. Here we examine the impact of a portable mosquito repeller, which emits prallethrin, a pyrethroid insecticide, on honey bee foraging and recruitment using a blinded, randomized, paired, parallel group trial. We found no significant effect of the volatilized insecticide on foraging frequency (our primary outcome), waggle dance propensity, waggle dance frequency, and feeder persistency (our secondary outcomes), even though an additional deposition study confirmed that the treatment device was performing appropriately. These results may be useful to consumers that are interested in repelling mosquitos, but also concerned about potential consequences to beneficial insects, such as honey bees.

Transcriptomic responses to location learning by honeybee dancers are partly mirrored in the brains of dance-followers.

The waggle dances of honeybees are a strikingly complex form of animal communication that underlie the collective foraging behaviour of colonies. The mechanisms by which bees assess the locations of forage sites that they have visited for representation on the dancefloor are now well-understood, but few studies have considered the remarkable backward translation of such information into flight vectors by dance-followers. Here, we explore whether the gene expression patterns that are induced through individual learning about foraging locations are mirrored when bees learn about those same locations from their nest-mates. We first confirmed that the mushroom bodies of honeybee dancers show a specific transcriptomic response to learning about distance, and then showed that approximately 5% of those genes were also differentially expressed by bees that follow dances for the same foraging sites, but had never visited them. A subset of these genes were also differentially expressed when we manipulated distance perception through an optic flow paradigm, and responses to learning about target direction were also in part mirrored in the brains of dance followers. Our findings show a molecular footprint of the transfer of learnt information from one animal to another through this extraordinary communication system, highlighting the dynamic role of the genome in mediating even very short-term behavioural changes.

Overcoming bias in the comparison of human language and animal communication.

Human language is a powerful communicative and cognitive tool. Scholars have long sought to characterize its uniqueness, but each time a property is proposed to set human language apart (e.g., reference, syntax), some (attenuated) version of that property is found in animals. Recently, the uniqueness argument has shifted from linguistic rules to cognitive capacities underlying them. Scholars argue that human language is unique because it relies on ostension and inference, while animal communication depends on simple associations and largely hardwired signals. Such characterizations are often borne out in published data, but these empirical findings are driven by radical differences in the ways animal and human communication are studied. The field of animal communication has been dramatically shaped by the "code model," which imagines communication as involving information packets that are encoded, transmitted, decoded, and interpreted. This framework standardized methods for studying meaning in animal signals, but it does not allow for the nuance, ambiguity, or contextual variation seen in humans. The code model is insidious. It is rarely referenced directly, but it significantly shapes how we study animals. To compare animal communication and human language, we must acknowledge biases resulting from the different theoretical models used. By incorporating new approaches that break away from searching for codes, we may find that animal communication and human language are characterized by differences of degree rather than kind.