Why Are No Animal Communication Systems Simple Languages?

Individuals of some animal species have been taught simple versions of human language despite their natural communication systems failing to rise to the level of a simple language. How is it, then, that some animals can master a version of language, yet none of them deploy this capacity in their own communication system? I first examine the key design features that are often used to evaluate language-like properties of natural animal communication systems. I then consider one candidate animal system, bird song, because it has several of the key design features or their precursors, including social learning and cultural transmission of their vocal signals. I conclude that although bird song communication is nuanced and complex, and has the acoustic potential for productivity, it is not productive - it cannot be used to say many different things. Finally, I discuss the debate over whether animal communication should be viewed as a cooperative information transmission process, as we typically view human language, or as a competitive process where signaler and receiver vie for control. The debate points to a necessary condition for the evolution of a simple language that has generally been overlooked: the degree of to which the interests of the signaler and receiver align. While strong cognitive and signal production mechanisms are necessary pre-adaptations for a simple language, they are not sufficient. Also necessary is the existence of identical or near-identical interests of signaler and receiver and a socio-ecology that requires high-level cooperation across a range of contexts. In the case of our hominid ancestors, these contexts included hunting, gathering, child care and, perhaps, warfare. I argue that the key condition for the evolution of human language was the extreme interdependency that existed among unrelated individuals in the hunter-gatherer societies of our hominid ancestors. This extreme interdependency produced multiple prosocial adaptations for effective intragroup cooperation, which in partnership with advanced cognitive abilities, set the stage for the evolution of language.

Social factors in bird-song development: Learning to sing with friends and rivals.

Laboratory studies have revealed that social factors are key in bird-song learning. Nevertheless, little is known about how or why birds choose the songs they do learn from the many they will hear under natural conditions. We focus on various theories concerning social song learning that have been offered to date, with special attention paid to two axes of social factors. First, does song learning occur via direct interaction of the young bird with song tutors, or via social eavesdropping by the young bird on interacting singers (social modeling of song)? Social modeling, a hypothesis first proposed by Pepperberg (Zeitschrift für Tierpsychologie, 55(2), 139-160, 1981), and direct interaction are not mutually exclusive hypotheses, and the evidence we review suggests both play a role in song learning. Second, does song learning occur via interactions with rivals (territorial competitors) or with friends (mutually tolerant or even cooperative territorial neighbors). These are largely mutually exclusive hypotheses, and can really only be tested in the field. There is little evidence on this contrast to date. We review our recent study on song sparrows, which indicates that both the young bird and his primary tutor may benefit from song learning/tutoring. If this mutual benefit result is confirmed by further studies, we believe that song "tutoring" in these cases may be more than a term of convenience: that it may qualify as true teaching.

Song sparrows do not discriminate between their own song and stranger song.

Bird song is socially learned. During song learning, the bird's hearing its own vocalization is important for normal development of song. Whether bird's own song is represented and recognized as a special category in adult birds, however, is unclear. If birds respond differently to their own songs when these are played back to them, this would be evidence for auditory self-recognition. To test this possibility, we presented song sparrow males (Melospiza melodia) playbacks of their own songs or stranger songs and measured aggressive responses as well as type matching. We found no evidence of behavioral discrimination of bird's own song relative to the (non-matching) stranger song. These findings cast doubt on an earlier proposal that song sparrows display auditory self-recognition and support the common assumption in playback experiments that bird's own song is perceived as stranger song.

Multi-modal communication: song sparrows increase signal redundancy in noise.

Although the effects of anthropogenic noise on animal communication have been studied widely, most research on the effect of noise in communication has focused on signals in a single modality. Consequently, how multi-modal communication is affected by anthropogenic noise is relatively poorly understood. Here, we ask whether song sparrows (Melospiza melodia) show evidence of plasticity in response to noise in two aggressive signals in acoustic and visual modalities. We test two hypotheses: (i) that song sparrows will shift signalling effort to the visual modality (the multi-modal shift hypothesis) and (ii) that they will increase redundancy of their multi-modal signalling (the back-up signal hypothesis). We presented male song sparrows with song playback and a taxidermic mount with or without a low-frequency acoustic noise from a nearby speaker. We found that males did not switch their signalling effort to visual modality (i.e. wing waves) in response to the noise. However, the correlation between warbled soft songs and wing waves increased in the noise treatment, i.e. signals became more redundant. These results suggest that when faced with anthropogenic noise, song sparrows can increase the redundancy of their multi-modal signals, which may aid in the robustness of the communication system.

The fitness consequences of honesty: Under-signalers have a survival advantage in song sparrows.

How honest or reliable signaling can evolve and be maintained has been a major question in evolutionary biology. The question is especially puzzling for a particular class of signals used in aggressive interactions: threat signals. Here, we report a study on song sparrows (Melospiza melodia) in which we assayed males with playbacks on their territories to quantify their aggressiveness (flights and close proximity) and aggressive signaling levels (rates of soft song, a close-range signal reliably predicting attack) and asked whether these traits affect individuals' survival on territory. We found that the effect of aggressive signaling via soft song interacted with aggressive behaviors such that there was a negative correlational selection: among males with low aggression, those males that signaled at higher levels (over-signalers) had higher survival whereas among males with high aggression those that signaled at low levels (under-signalers) survived longer. In other words, males that deviate from reliable signaling have a survival advantage. These results, along with previous research that suggested most of the deviation from reliable signaling in this system is in the form of under-signaling (high-aggression males signaling at low levels) pose a puzzle for future research on how this reliable signaling system is maintained.

Individual differences affect honest signalling in a songbird.

Research in the past decade has established the existence of consistent individual differences or 'personality' in animals and their important role in many aspects of animal behaviour. At the same time, research on honest signalling of aggression has revealed that while some of the putative aggression signals are reliable, they are only imperfectly so. This study asks whether a significant portion of the variance in the aggression-signal regression may be explained by individual differences in signalling strategies. Using the well-studied aggressive signalling system of song sparrows (Melospiza melodia), we carried out repeated assays to measure both aggressive behaviours and aggressive signalling of territorial males. Through these assays, we found that aggressive behaviours and aggressive signalling were both highly repeatable, and moreover that aggressive behaviours in 2009-2010 predicted whether the birds would attack a taxidermic mount over a year later. Most significantly, we found that residual variation in signalling behaviours, after controlling for aggressive behaviour, was individually consistent, suggesting there may be a second personality trait determining the level of aggressive signalling. We term this potential personality trait 'communicativeness' and discuss these results in the context of honest signalling theories and recent findings reporting prevalence of 'under-signalling'.

Song type matching is an honest early threat signal in a hierarchical animal communication system.

Aggressive encounters between animals often involve significant amounts of signalling before or in lieu of physical fights. When, as is often the case, these apparent threat signals are neither inherently costly nor inherently indicative of fighting ability, we should ask whether they are in fact honest signals, i.e. do they predict that escalation is imminent? While signalling theories have indicated that such 'conventional' threat signals can honestly predict escalation, attempts to gather supporting empirical evidence have mostly failed. For example, recent studies in songbirds of song type matching (replying to an opponent's song with the same song type he has just sung) have failed to confirm that it predicts an eventual attack by the signaller. In the present study of song sparrows (Melospiza melodia), we tested the hypothesis that song type matching is an early threat signal in a hierarchical signalling system. We used an improved model-playback design that simulated an escalating intrusion onto the subject's territory: the simulated opponent first sang in hiding from the boundary before moving to the centre of the territory, where he revealed himself and continued to sing. We found that type matching beginning in the boundary phase and continuing into the escalation phase, or beginning immediately after the escalation, reliably predicted both subsequent escalated signalling (soft songs and wing waves) and subsequent attack on the model, supporting the hypothesis that type matching is a reliable early threat signal.

Spatial movements and social networks in juvenile male song sparrows.

The time between fledging and breeding is a critical period in songbird ontogeny, but the behavior of young songbirds in the wild is relatively unstudied. The types of social relationships juveniles form with other individuals can provide insight into the process through which they learn complex behaviors crucial for survival, territory establishment, and mate attraction. We used radio telemetry to observe social associations of young male song sparrows (Melospiza melodia) from May to November. Juvenile song sparrows were frequently observed in social flocks and generally associated with more birds in the summer than in the autumn months. Most juvenile subjects formed stable social relationships with other birds and were seen with the same individual on up to 60% of the days observed. The strongest associations occurred with other juvenile males, and these individuals were often seen <1 m from the subject, even when the subject moved large distances between tracking observations. Associations also had long-term behavioral consequences as subjects were more likely to establish territories near their associates and learn shared song types. Our results indicate that male song sparrows spend a large percentage of the juvenile life stage forming social relationships and suggest that these associations may be important for the ecology of young birds and the ontogeny of their behaviors.

Immediate and long-term effects of testosterone on song plasticity and learning in juvenile song sparrows.

Steroid sex hormones play critical roles in the development of brain regions used for vocal learning. It has been suggested that puberty-induced increases in circulating testosterone (T) levels crystallize a bird's repertoire and inhibit future song learning. Previous studies show that early administration of T crystallizes song repertoires but have not addressed whether new songs can be learned after this premature crystallization. We brought 8 juvenile song sparrows (Melospiza melodia) into the laboratory in the late summer and implanted half of them with subcutaneous T pellets for a two week period in October. Birds treated with T tripled their singing rates and crystallized normal songs in 2 weeks. After T removal, subjects were tutored by 4 new adults. Birds previously treated with T tended toward learning fewer new songs post T, consistent with the hypothesis that T helps to close the song learning phase. However, one T-treated bird proceeded to learn several new songs in the spring, despite singing perfectly crystallized songs in the fall. His small crystallized fall repertoire and initial lag behind other subjects in song development suggest that this individual may have had limited early song learning experience. We conclude that an exposure to testosterone sufficient for crystallization of a normal song repertoire does not necessarily prevent future song learning and suggest that early social experiences might override the effects of hormones in closing song learning.

Juvenile sparrows preferentially eavesdrop on adult song interactions.

Recent research has demonstrated that bird song learning is influenced by social factors, but so far has been unable to isolate the particular social variables central to the learning process. Here we test the hypothesis that eavesdropping on singing interactions of adults is a key social event in song learning by birds. In a field experiment, we compared the response of juvenile male song sparrows (Melospiza melodia) to simulated adult counter-singing versus simulated solo singing. We used radio telemetry to follow the movements of each focal bird and assess his response to each playback trial. Juveniles approached the playback speakers when exposed to simulated interactive singing of two song sparrows, but not when exposed to simulated solo singing of a single song sparrow, which in fact they treated similar to heterospecific singing. Although the young birds approached simulated counter-singing, neither did they approach closely, nor did they vocalize themselves, suggesting that the primary function of approach was to permit eavesdropping on these singing interactions. These results indicate that during the prime song-learning phase, juvenile song sparrows are attracted to singing interactions between adults but not to singing by a single bird and suggest that singing interactions may be particularly powerful song-tutoring events.

Song learning in birds: diversity and plasticity, opportunities and challenges.

A common trend in neuroscience is convergence on selected model systems. Underlying this approach is an often implicit assumption that mechanisms observed in one species are characteristic of all related species. Although the model system approach has been extremely productive, it might not account for all of the mechanistic differences between species that differ behaviourally. Using the neural system that regulates song learning in songbirds as an example, we demonstrate how integrating model system and comparative approaches can lead to a more complete picture of neural mechanisms, and can resolve issues raised by a focus on selected species.

Functional aspects of song learning in songbirds.

The oscine passerines, or 'songbirds', are one of the few animal taxa in which individuals learn their vocal signals. Recent comparative studies reveal a remarkable diversity of song-learning strategies in the songbirds. Here, we discuss recent studies that shed light on the possible functional basis of different song-learning programs. We argue that further insights into the evolution and ecology of song learning will require that comparative data and functional hypotheses be analyzed in a phylogenetic context, and we review recent studies that we feel might be the first steps in this process.

Seasonal changes in avian song control circuits do not cause seasonal changes in song discrimination in song sparrows.

In seasonally breeding songbirds, brain nuclei of the song control system that act in song perception change in size between seasons. It has been hypothesized that seasonal regression of song nuclei may impair song discrimination. We tested this hypothesis in song sparrows (Melospiza melodia), a species in which males share song types with neighbors and must discriminate between similar songs in territorial interactions. We predicted that song sparrows with regressed song systems would have greater difficulty in discriminating between similar songs. Sparrows were housed either on short days (SD) and had regressed song circuits, or were exposed to long days and implanted with testosterone (LD+T) to induce full growth of the song circuits. We conducted two experiments using a GO/NO-GO operant conditioning paradigm to measure song discrimination ability of each group. Birds learned four (experiment 1) or three (experiment 2) pairs of song types sequentially, with each pair more similar in the number of shared song elements and thus more difficult to discriminate. Circulating T levels differed between the SD and LD+T groups. The telencephalic song nuclei HVc, RA, and area X were larger in the LD+T birds. The two groups of sparrows did not differ, however, in their ability to learn to discriminate between shared song types, regardless of the songs' similarity. These results suggest that seasonal changes in the song control system do not affect birds' ability to make difficult song discriminations.