Toshitaka N. Suzuki

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

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

Kinship modulates the attention of naïve individuals to the mobbing behaviour of role models

The social acquisition of life skills is essential in a wide range of species. Field experiments have demonstrated that naive young learn particularly from their parents how to deal with predators or how to find suitable food. However, it remains unclear whether the response of young differs in a novel situation when together with related (i.e. parents) or unrelated role models. We addressed this question in a group-living bird species, the Siberian jay, Perisoreus infaustus , groups of which can contain both related and unrelated juveniles. Groups are formed around a breeding pair which engages in prolonged parental care, facilitating delayed dispersal of offspring for up to 5 years. About 25% of juveniles are killed by predators during their first year of life, suggesting that predator avoidance is a crucial life skill for juveniles. Exposing groups to perched predator models showed that kinship influenced how juveniles responded to the mobbing behaviour of breeders. Upon exposure to a predator model, related juveniles immediately paid attention to the behaviour of breeders and copied most of their movements. In contrast, unrelated juveniles copied the behaviour of breeders less frequently, but regularly foraged in the presence of a predator model. These results show that juveniles respond differently to parents and unrelated role models, potentially affecting the acquisition of vital life skills. Parental care creates a close social bond, predisposing juveniles to pay attention especially to novel behaviours shown by their care-givers. Furthermore, parents have a fitness benefit from facilitating the skill acquisition of their offspring. Thus, a prolonged parent-offspring association is likely to enhance skill acquisition and influence cognitive evolution across species.

Referential calls coordinate multi-species mobbing in a forest bird community

Japanese great tits (Parus minor) use a sophisticated system of anti-predator communication when defending their offspring: they produce different mobbing calls for different nest predators (snake versus non-snake predators) and thereby convey this information to conspecifics (i.e. functionally referential call system). The present playback experiments revealed that these calls also serve to coordinate multi-species mobbing at nests; snake-specific mobbing calls attracted heterospecific individuals close to the sound source and elicited snake-searching behaviour, whereas non-snake mobbing calls attracted these birds at a distance. This study demonstrates for the first time that referential mobbing calls trigger different formations of multi-species mobbing parties.

Wild Birds Use an Ordering Rule to Decode Novel Call Sequences

The generative power of human language depends on grammatical rules, such as word ordering, that allow us to produce and comprehend even novel combinations of words [1-3]. Several species of birds and mammals produce sequences of calls [4-6], and, like words in human sentences, their order may influence receiver responses [7]. However, it isxa0unknown whether animals use call ordering to extract meaning from truly novel sequences. Here, we use a novel experimental approach to test this in a wild bird species, the Japanese tit (Parus minor). Japanese tits are attracted to mobbing a predator when they hear conspecific alert and recruitment calls ordered as alert-recruitment sequences [7]. They also approach in response to recruitment calls of heterospecific individuals in mixed-species flocks [8, 9]. Using experimental playbacks, we assess their responses to artificial sequences in which their own alert calls are combined into different orderings with heterospecific recruitment calls. We find that Japanese tits respond similarly to mixed-species alert-recruitment call sequences and to their own alert-recruitment sequences. Importantly, however, tits rarely respond to mixed-species sequences inxa0which the call order is reversed. Thus, Japanese tits extract a compound meaning from novel call sequences using an ordering rule. These results demonstrate a new parallel between animal communication systems and human language, opening new avenues for exploring the evolution of ordering rules and compositionality in animal vocal sequences.

Bent posture improves the protective value of bird dropping masquerading by caterpillars

Masquerade describes a defence by animals that have evolved to closely resemble inedible objects such as twigs, stones or bird droppings. Animals that masquerade often match their models in size or shape, and may even adopt specific postures in order to enhance their resemblance, causing predators to misclassify them as their model objects. The caterpillars of some moth species resemble bird droppings, and bend their bodies while resting on branches or leaves. We hypothesized that such bending might enhance the caterpillars resemblance to real bird droppings. In this study, we tested this hypothesis by pinning artificial caterpillars with green or bird dropping coloration onto tree branches in both straight and bent postures, after which we exposed them to bird predation in the wild. We found that the adoption of a bent posture resulted in a lower attack rate by birds on the artificial caterpillars with the bird dropping coloration, while green caterpillars experienced no benefit from the same treatment. This study is the first experimental demonstration of the protective value of a specific posture in masquerading prey, and highlights the importance of considering an organisms shape and posture in the study of masquerade.

Foraging intention affects whether willow tits call to attract members of mixed-species flocks

Understanding how individual behaviour influences the spatial and temporal distribution of other species is necessary to resolve the complex structure of species assemblages. Mixed-species bird flocks provide an ideal opportunity to investigate this issue, because members of the flocks are involved in a variety of behavioural interactions between species. Willow tits (Poecile montanus) often produce loud calls when visiting a new foraging patch to recruit other members of mixed-species flocks. The costs and benefits of flocking would differ with individual foraging behaviours (i.e. immediate consumption or caching); thus, willow tits may adjust the production of loud calls according to their foraging intention. In this study, we investigated the link between foraging decisions and calling behaviour in willow tits and tested its influence on the temporal cohesion with members of mixed-species flocks. Observations at experimental foraging patches showed that willow tits produced more calls when they consumed food items compared with when they cached them. Playback experiments revealed that these calls attracted flock members and helped to maintain their presence at foraging patches. Thus, willow tits adjusted calling behaviour according to their foraging intention, thereby coordinating the associations with members of mixed-species flocks. Our findings demonstrate the influence of individual decision-making on temporal cohesion with other species and highlight the importance of interspecific communication in mixed-species flocking dynamics.

Alarm calls evoke a visual search image of a predator in birds

Significance In human speech, words often cause listeners to retrieve visual mental images of target objects. In nonhuman animal communication systems, many key, language-like features have been demonstrated, but there is still no evidence that animal signals evoke mental images of objects in receivers. Japanese tits produce specific alarm calls when encountering a predatory snake. Here, I show that simply hearing these calls causes tits to become more visually perceptive to objects resembling snakes (moving sticks). This result indicates that before having detected a real snake, tits retrieve its visual image from snake-specific alarm calls and uses this to search out snakes. This study provides evidence for a call-evoked visual search image in a nonhuman animal. One of the core features of human speech is that words cause listeners to retrieve corresponding visual mental images. However, whether vocalizations similarly evoke mental images in animal communication systems is surprisingly unknown. Japanese tits (Parus minor) produce specific alarm calls when and only when encountering a predatory snake. Here, I show that simply hearing these calls causes tits to become more visually perceptive to objects resembling snakes. During playback of snake-specific alarm calls, tits approach a wooden stick being moved in a snake-like fashion. However, tits do not respond to the same stick when hearing other call types or if the stick’s movement is dissimilar to that of a snake. Thus, before detecting a real snake, tits retrieve its visual image from snake-specific alarm calls and use this to search out snakes. This study provides evidence for a call-evoked visual search image in a nonhuman animal, offering a paradigm to explore the cognitive basis for animal vocal communication in the wild.

Occasional cooperative breeding in birds and the robustness of comparative analyses concerning the evolution of cooperative breeding

Cooperative breeding is a widespread and intense form of cooperation, in which individuals help raise offspring that are not their own. This behaviour is particularly well studied in birds, using both long-term and comparative studies that have provided insights into the evolution of reproductive altruism. In most cooperatively breeding species, helpers are offspring that remain with their parents beyond independency and help in the raising of younger siblings. However, many cooperatively breeding species are poorly studied, and in 152 species, this behaviour only has been observed infrequently (i.e., occasional cooperative breeding). Here we argue that the parental care mode of these 152 species needs to be treated with caution, as factors associated with occasional cooperative breeding may differ from those associated with “regular” cooperative breeding. In most cooperatively breeding species, helpers provide alloparental care at the nests of their parents or close relatives; however, only in one occasionally cooperatively breeding species do offspring remain into the next breeding season with their parents. Accordingly, different factors are likely to be associated with regular and occasional cooperative breeding. The latter behaviour resembles interspecific feeding (i.e., individuals feed offspring of another species), which occurs when birds lose their brood and begin feeding at a nearby nest, or when birds mistakenly feed at another nest. Thus, we advise researchers to exclude occasional cooperative breeders in comparative analyses until their status is clarified, or to categorize them separately or according to the typically observed parental care mode. This approach will increase the robustness of comparative analyses and thereby improve our understanding of factors that drive the evolution of cooperative breeding.

Call combinations in birds and the evolution of compositional syntax

Syntax is the set of rules for combining words into phrases, providing the basis for the generative power of linguistic expressions. In human language, the principle of compositionality governs how words are combined into a larger unit, the meaning of which depends on both the meanings of the words and the way in which they are combined. This linguistic capability, i.e., compositional syntax, has long been considered a trait unique to human language. Here, we review recent studies on call combinations in a passerine bird, the Japanese tit (Parus minor), that provide the first firm evidence for compositional syntax in a nonhuman animal. While it has been suggested that the findings of these studies fail to provide evidence for compositionality in Japanese tits, this criticism is based on misunderstanding of experimental design, misrepresentation of the importance of word order in human syntax, and necessitating linguistic capabilities beyond those given by the standard definition of compositionality. We argue that research on avian call combinations has provided the first steps in elucidating how compositional expressions could have emerged in animal communication systems.

From bird calls to human language: exploring the evolutionary drivers of compositional syntax

Compositional syntax, where lexical items are combined into larger units, has been assumed to be unique to human language. Recent experiments, however, showed that Japanese tits combine alert and recruitment calls into alert-recruitment sequences when attracting conspecifics to join in mobbing a predator. We speculate that such call combinations are favoured when: Firstly, callers and receivers have shared interests in exchanging information; secondly, species produce different types of calls in different situations, leading to distinct behavioural responses in receivers; and finally, complex situations exist in which receivers benefit by combining two or more behaviours. These preconditions were also present in human ancestors. Thus, future work on bird calls may provide insights into the evolution of compositional syntax in human language.