Naive poison frog tadpoles use bi-modal cues to avoid insect predators but not heterospecific predatory tadpoles.

For animals to survive until reproduction, it is crucial that juveniles successfully detect potential predators and respond with appropriate behavior. The recognition of cues originating from predators can be innate or learned. Cues of various modalities might be used alone or in multi-modal combinations to detect and distinguish predators but studies investigating multi-modal integration in predator avoidance are scarce. Here, we used wild, naive tadpoles of the Neotropical poison frog Allobates femoralis ( Boulenger, 1884) to test their reaction to cues with two modalities from two different sympatrically occurring potential predators: heterospecific predatory Dendrobates tinctorius tadpoles and dragonfly larvae. We presented A. femoralis tadpoles with olfactory or visual cues, or a combination of the two, and compared their reaction to a water control in a between-individual design. In our trials, A. femoralis tadpoles reacted to multi-modal stimuli (a combination of visual and chemical information) originating from dragonfly larvae with avoidance but showed no reaction to uni-modal cues or cues from heterospecific tadpoles. In addition, visual cues from conspecifics increased swimming activity while cues from predators had no effect on tadpole activity. Our results show that A. femoralis tadpoles can innately recognize some predators and probably need both visual and chemical information to effectively avoid them. This is the first study looking at anti-predator behavior in poison frog tadpoles. We discuss how parental care might influence the expression of predator avoidance responses in tadpoles.

Early life differences in behavioral predispositions in two Alligatoridae species.

Behavioral predispositions are innate tendencies of animals to behave in a given way without the input of learning. They increase survival chances and, due to environmental and ecological challenges, may vary substantially even between closely related taxa. These differences are likely to be especially pronounced in long-lived species like crocodilians. This order is particularly relevant for comparative cognition due to its phylogenetic proximity to birds. Here we compared early life behavioral predispositions in two Alligatoridae species. We exposed American alligator and spectacled caiman hatchlings to three different novel situations: a novel object, a novel environment that was open and a novel environment with a shelter. This was then repeated a week later. During exposure to the novel environments, alligators moved around more and explored a larger range of the arena than the caimans. When exposed to the novel object, the alligators reduced the mean distance to the novel object in the second phase, while the caimans further increased it, indicating diametrically opposite ontogenetic development in behavioral predispositions. Although all crocodilian hatchlings face comparable challenges, e.g., high predation pressure, the effectiveness of parental protection might explain the observed pattern. American alligators are apex predators capable of protecting their offspring against most dangers, whereas adult spectacled caimans are frequently predated themselves. Their distancing behavior might be related to increased predator avoidance and also explain the success of invasive spectacled caimans in the natural habitats of other crocodilians.

Common marmosets are sensitive to simple dependencies at variable distances in an artificial grammar.

Recognizing that two elements within a sequence of variable length depend on each other is a key ability in understanding the structure of language and music. Perception of such interdependencies has previously been documented in chimpanzees in the visual domain and in human infants and common squirrel monkeys with auditory playback experiments, but it remains unclear whether it typifies primates in general. Here, we investigated the ability of common marmosets (Callithrix jacchus) to recognize and respond to such dependencies. We tested subjects in a familiarization-discrimination playback experiment using stimuli composed of pure tones that either conformed or did not conform to a grammatical rule. After familiarization to sequences with dependencies, marmosets spontaneously discriminated between sequences containing and lacking dependencies ('consistent' and 'inconsistent', respectively), independent of stimulus length. Marmosets looked more often to the sound source when hearing sequences consistent with the familiarization stimuli, as previously found in human infants. Crucially, looks were coded automatically by computer software, avoiding human bias. Our results support the hypothesis that the ability to perceive dependencies at variable distances was already present in the common ancestor of all anthropoid primates (Simiiformes).

A technological framework for running and analyzing animal head turning experiments.

Head turning experiments are widely used to test the cognition of both human infants and non-human animal species. Monitoring head turns allows researchers to non-invasively assess attention to acoustic or visual stimuli. In the majority of head turning experiments, the head direction analyses have been accomplished manually, which is extremely labor intensive and can be affected by subjectivity or other human errors and limitations. In the current study, we introduce an open-source computer program for measuring head directions of freely moving animals including common marmoset monkeys (Callithrix jacchus), American alligators (Alligator mississippiensis), and Mongolian gerbils (Meriones unguiculatus) to reduce human effort and time in video coding. We also illustrate an exemplary framework for an animal head turning experiment with common marmoset monkeys. This framework incorporates computer-aided processes of data acquisition, preprocessing, and analysis using the aforementioned software and additional open-source software and hardware.

Humans recognize emotional arousal in vocalizations across all classes of terrestrial vertebrates: evidence for acoustic universals.

Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes-Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system.

A Chinese alligator in heliox: formant frequencies in a crocodilian.

Crocodilians are among the most vocal non-avian reptiles. Adults of both sexes produce loud vocalizations known as 'bellows' year round, with the highest rate during the mating season. Although the specific function of these vocalizations remains unclear, they may advertise the caller's body size, because relative size differences strongly affect courtship and territorial behaviour in crocodilians. In mammals and birds, a common mechanism for producing honest acoustic signals of body size is via formant frequencies (vocal tract resonances). To our knowledge, formants have to date never been documented in any non-avian reptile, and formants do not seem to play a role in the vocalizations of anurans. We tested for formants in crocodilian vocalizations by using playbacks to induce a female Chinese alligator (Alligator sinensis) to bellow in an airtight chamber. During vocalizations, the animal inhaled either normal air or a helium/oxygen mixture (heliox) in which the velocity of sound is increased. Although heliox allows normal respiration, it alters the formant distribution of the sound spectrum. An acoustic analysis of the calls showed that the source signal components remained constant under both conditions, but an upward shift of high-energy frequency bands was observed in heliox. We conclude that these frequency bands represent formants. We suggest that crocodilian vocalizations could thus provide an acoustic indication of body size via formants. Because birds and crocodilians share a common ancestor with all dinosaurs, a better understanding of their vocal production systems may also provide insight into the communication of extinct Archosaurians.

Social monitoring via close calls in meerkats.

Social monitoring of the actions of group members is thought to be a key development associated with group living. Humans constantly monitor the behaviour of others and respond to them in a flexible way depending on past interactions and the current social context. While other primates have also been reported to change their behaviour towards other group members flexibly based on the current state of their relationship, empirical evidence is typically linked to contextually specific events such as aggressive or reproductive interactions. In the cooperatively breeding meerkat (Suricata suricatta), we investigated whether subordinate females use frequently emitted, non-agonistic close calls to monitor the location of the dominant female and whether they subsequently adjust their response based on recent social interactions during conflict and non-conflict periods. Subjects discriminated between the close calls of the dominant female and control playbacks, responding by approaching the loudspeaker and displaying submissive behaviour only if they were currently threatened by eviction. Our results suggest that meerkats assess the risk for aggressive interactions with close associates depending on social circumstances, and respond accordingly. We argue that social monitoring based on non-agonistic cues is probably a common mechanism in group-living species that allows the adjustment of behaviour depending on variation in relationships.

Gaze following in Archosauria-Alligators and palaeognath birds suggest dinosaur origin of visual perspective taking.

Taking someone else's visual perspective marks an evolutionary shift in the formation of advanced social cognition. It enables using others' attention to discover otherwise hidden aspects of the surroundings and is foundational for human communication and understanding of others. Visual perspective taking has also been found in some other primates, a few songbirds, and some canids. However, despite its essential role for social cognition, visual perspective taking has only been fragmentedly studied in animals, leaving its evolution and origins uncharted. To begin to narrow this knowledge gap, we investigated extant archosaurs by comparing the neurocognitively least derived extant birds-palaeognaths-with the closest living relatives of birds, the crocodylians. In a gaze following paradigm, we showed that palaeognaths engage in visual perspective taking and grasp the referentiality of gazes, while crocodylians do not. This suggests that visual perspective taking originated in early birds or nonavian dinosaurs-likely earlier than in mammals.

Socio-ecological correlates of neophobia in corvids.

Behavioral responses to novelty, including fear and subsequent avoidance of novel stimuli, i.e., neophobia, determine how animals interact with their environment. Neophobia aids in navigating risk and impacts on adaptability and survival. There is variation within and between individuals and species; however, lack of large-scale, comparative studies critically limits investigation of the socio-ecological drivers of neophobia. In this study, we tested responses to novel objects and food (alongside familiar food) versus a baseline (familiar food alone) in 10 corvid species (241 subjects) across 10 labs worldwide. There were species differences in the latency to touch familiar food in the novel object and novel food conditions relative to the baseline. Four of seven socio-ecological factors influenced object neophobia: (1) use of urban habitat (versus not), (2) territorial pair versus family group sociality, (3) large versus small maximum flock size, and (4) moderate versus specialized caching (whereas range, hunting live animals, and genus did not), while only maximum flock size influenced food neophobia. We found that, overall, individuals were temporally and contextually repeatable (i.e., consistent) in their novelty responses in all conditions, indicating neophobia is a stable behavioral trait. With this study, we have established a network of corvid researchers, demonstrating potential for further collaboration to explore the evolution of cognition in corvids and other bird species. These novel findings enable us, for the first time in corvids, to identify the socio-ecological correlates of neophobia and grant insight into specific elements that drive higher neophobic responses in this avian family group. VIDEO ABSTRACT.

Hear them roar: A comparison of black-capped chickadee (Poecile atricapillus) and human (Homo sapiens) perception of arousal in vocalizations across all classes of terrestrial vertebrates.

Recently, evidence for acoustic universals in vocal communication was found by demonstrating that humans can identify levels of arousal in vocalizations produced by species across three biological classes (Filippi et al., 2017). Here, we extend this work by testing whether two vocal learning species, humans and chickadees, can discriminate vocalizations of high and low arousal using operant discrimination go/no-go tasks. Stimuli included vocalizations from nine species: giant panda, American alligator, common raven, hourglass treefrog, African elephant, Barbary macaque, domestic pig, black-capped chickadee, and human. Subjects were trained to respond to high or low arousal vocalizations, then tested with additional high and low arousal vocalizations produced by each species. Chickadees (Experiment 1) and humans (Experiment 2) learned to discriminate between high and low arousal stimuli and significantly transferred the discrimination to additional panda, human, and chickadee vocalizations. Finally, we conducted discriminant function analyses using four acoustic measures, finding evidence suggesting that fundamental frequency played a role in responding during the task. However, these analyses also suggest roles for other acoustic factors as well as familiarity. In sum, the results from these studies provide evidence that chickadees and humans are capable of perceiving arousal in vocalizations produced by multiple species. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Formants provide honest acoustic cues to body size in American alligators.

In many vertebrates, acoustic cues to body size are encoded in resonance frequencies of the vocal tract ("formants"), rather than in the rate of tissue vibration in the sound source ("pitch"). Anatomical constraints on the vocal tract's size render formants honest cues to size in many bird and mammal species, but it is not clear whether this correlation evolved convergently in these two clades, or whether it is widespread among amniotes (mammals, birds, and non-avian reptiles). We investigated the potential for honest acoustic cues in the bellows of adult American alligators and found that formant spacing provided highly reliable cues to body size, while presumed correlates of the source signal did not. These findings held true for both sexes and for all bellows whether produced in or out of water. Because birds and crocodilians are the last extant Archosaurians and share common ancestry with all extinct dinosaurs, our findings support the hypothesis that dinosaurs used formants as cues to body size. The description of formants as honest signals in a non-avian reptile combined with previous evidence from birds and mammals strongly suggests that the principle of honest signalling via vocal tract resonances may be a broadly shared trait among amniotes.

Ravens attribute visual access to unseen competitors.

Recent studies purported to demonstrate that chimpanzees, monkeys and corvids possess a basic Theory of Mind, the ability to attribute mental states like seeing to others. However, these studies remain controversial because they share a common confound: the conspecific's line of gaze, which could serve as an associative cue. Here, we show that ravens Corvus corax take into account the visual access of others, even when they cannot see a conspecific. Specifically, we find that ravens guard their caches against discovery in response to the sounds of conspecifics when a peephole is open but not when it is closed. Our results suggest that ravens can generalize from their own perceptual experience to infer the possibility of being seen. These findings confirm and unite previous work, providing strong evidence that ravens are more than mere behaviour-readers.

Territorial raven pairs are sensitive to structural changes in simulated acoustic displays of conspecifics.

Human language involves combining items into meaningful, syntactically structured wholes. The evolutionary origin of syntactic abilities has been investigated by testing pattern perception capacities in nonhuman animals. New World primates can respond spontaneously to structural changes in acoustic sequences and songbirds can learn to discriminate between various patterns in operant tasks. However, there is no conclusive evidence that songbirds respond spontaneously to structural changes in patterns without reinforcement or training. In this study, we tested pattern perception capacities of common ravens, Corvus corax, in a habituation-discrimination playback experiment. To enhance stimulus salience, call recordings of male and female ravens were used as acoustic elements, combined to create artificial territorial displays as target patterns. We habituated captive territorial raven pairs to displays following a particular pattern and subsequently exposed them to several test and control playbacks. Subjects spent more time visually orienting towards the loudspeaker in the discrimination phase when they heard structurally novel call combinations, violating the pattern presented during habituation. This demonstrates that songbirds, much like primates, can be sensitive to structural changes in auditory patterns and respond to them spontaneously, without training.