The use of network analysis to study complex animal communication systems: a study on nightingale song.

The singing of song birds can form complex signal systems comprised of numerous subunits sung with distinct combinatorial properties that have been described as syntax-like. This complexity has inspired inquiries into similarities of bird song to human language; but the quantitative analysis and description of song sequences is a challenging task. In this study, we analysed song sequences of common nightingales (Luscinia megarhynchos) by means of a network analysis. We translated long nocturnal song sequences into networks of song types with song transitions as connectors. As network measures, we calculated shortest path length and transitivity and identified the 'small-world' character of nightingale song networks. Besides comparing network measures with conventional measures of song complexity, we also found a correlation between network measures and age of birds. Furthermore, we determined the numbers of in-coming and out-going edges of each song type, characterizing transition patterns. These transition patterns were shared across males for certain song types. Playbacks with different transition patterns provided first evidence that these patterns are responded to differently and thus play a role in singing interactions. We discuss potential functions of the network properties of song sequences in the framework of vocal leadership. Network approaches provide biologically meaningful parameters to describe the song structure of species with extremely large repertoires and complex rules of song retrieval.

Memory-dependent adjustment of vocal response latencies in a territorial songbird.

Vocal interactions in songbirds can be used as a model system to investigate the interplay of intrinsic singing programmes (e.g. influences from vocal memories) and external variables (e.g. social factors). When characterizing vocal interactions between territorial rivals two aspects are important: (1) the timing of songs in relation to the conspecific's singing and (2) the use of a song pattern that matches the rival's song. Responses in both domains can be used to address a territorial rival. This study is the first to investigate the relation of the timing of vocal responses to (1) the vocal memory of a responding subject and (2) the selection of the song pattern that the subject uses as a response. To this end, we conducted interactive playback experiments with adult nightingales (Luscinia megarhynchos) that had been hand-reared and tutored in the laboratory. We analysed the subjects' vocal response latencies towards broadcast playback stimuli that they either had in their own vocal repertoire (songs shared with playback) or that they had not heard before (unknown songs). Likewise, we compared vocal response latencies between responses that matched the stimulus song and those that did not. Our findings showed that the latency of singing in response to the playback was shorter for shared versus unknown song stimuli when subjects overlapped the playback stimuli with their own song. Moreover birds tended to overlap faster when vocally matching the stimulus song rather than when replying with a non-matching song type. We conclude that memory of song patterns influenced response latencies and discuss possible mechanisms.

Rules of song development and their use in vocal interactions by birds with large repertoires.

Songbirds are well known for settling their disputes by vocal signals, and their singing plays a dominant role. Most studies on this issue have concentrated on bird species that develop and use small vocal repertoires. In this article we will go farther and focus on examples of how species with large song repertoires make use of their vocal competence. In particular, we will outline the study of interaction rules which have been elucidated by examining time- and pattern-specific relationships between signals exchanged by territorial neighbors. First we present an inquiry into the rules of song learning and development. In birds with large song repertoires, the ontogeny of such rules proceeds along a number of trajectories which help in understanding the often remarkable accomplishments of adult birds. In both approaches, our model species will be the Common Nightingale Luscinia megarhynchos that has been investigated intensively in the field and in the laboratory.

Approaches to the mechanisms of song memorization and singing provide evidence for a procedural memory.

There is growing evidence that, during song learning, birds do not only acquire 'what to sing' (the inventory of behavior), but also 'how to sing' (the singing program), including order-features of song sequencing. Common Nightingales Luscinia megarhynchos acquire such serial information by segmenting long strings of heard songs into smaller subsets or packages, by a process reminiscent of the chunking of information as a coding mechanism in short term memory. Here we report three tutoring experiments on nightingales that examined whether such 'chunking' was susceptible to experimental cueing. The experiments tested whether (1) 'temporal phrasing' (silent intersong intervals spaced out at particular positions of a tutored string), or (2) 'stimulus novelty' (groups of novel song-types added to a basic string), or (3) 'pattern similarity' in the phonetic structure of songs (here: sharing of song initials) would induce package boundaries (or chunking) at the manipulated sequential positions. The results revealed cueing effects in experiments (1) and (2) but not in experiment (3). The finding that birds used temporal variables as cues for chunking does not require the assumption that package formation is a cognitive strategy. Rather, it points towards a mechanism of procedural memory operating in the song acquisition of birds.

Approaches to the mechanisms of song memorization and singing provide evidence for a procedural memory

Há evidências crescentes de que, durante a aprendizagem do canto, as aves adquirem não somente "o que cantar" (o repertório comportamental), mas também "como cantar" (o programa do canto), incluindo regras de seqüência do canto. O Rouxinol-comum Luscinia megarhynchos adquire essas informaçäes seriadas dividindo as longas cadeias de cantos ouvidos em segmentos ou pacotes menores através de um processo lembrando o corte ("chunking") de informação como mecanismo codificador na memória de curto prazo. Aqui relatamos três experimentos de aprendizagem pelo rouxinol para ver se tal "chunking" é suscetível de marcação experimental. Os experimentos testaram se (1) a "articulação temporal" (intervalos de silêncio entre cantos repartidos em determinadas posiçäes na série aprendida), ou (2) a "novidade do estímulo" (grupos de novos tipos de canto acrescidos a uma série básica), ou (3) a "similaridade de padrão" na estrutura fonética do canto (aqui o mesmo início dos cantos) induziria os limites dos pacotes (ou seja o "chunking") nas posiçäes seqüenciais definidas experimentalmente. Os resultados mostram efeitos de marcação nos experimentos (1) e (2), mas não no (3). A descoberta de que as aves usam variáveis temporais como marcas para o "chunking" não exige assumir que a formação dos pacotes seja uma estratégia cognitiva. Isto melhor indica que um mecanismo de memória procedural opera na aquisição do canto das aves.

Rules of song development and their use in vocal interactions by birds with large repertoires

Pássaros canoros são bem conhecidos por resolver suas brigas através de sinais vocais e seu canto tem um papel dominante. A maioria dos estudos sobre este assunto focalizou espécies de aves que desenvolvem e usam repertórios vocais pequenos. Neste artigo iremos mais longe, examinando como espécies com grandes repertórios fazem uso de suas capacidades. Descreveremos particularmente o estudo das regras de interação que foram desvendadas pelo exame das relaçäes temporais e estruturais entre os sinais trocados por vizinhos. Inicialmente, investigamos as regras de aprendizagem e desenvolvimento do canto. Nas aves com grande repertório vocal, a ontogênese dessas regras segue certas trajetórias que ajudam a entender o desempenho dos adultos, geralmente notável. Em ambas abordagens, nossa espécie-modelo será o Rouxinol-comum Luscinia megarhynchos, que foi pesquisado intensamente no campo e no laboratório.

Long-time storage of song types in birds: evidence from interactive playbacks.

In studies of birdsong learning, imitation-based assays of stimulus memorization do not take into account that tutored song types may have been stored, but were not retrieved from memory. Such a 'silent' reservoir of song material could be used later in the bird's life, e.g. during vocal interactions. We examined this possibility in hand-reared nightingales during their second year. The males had been exposed to songs, both as fledglings and later, during their first full song period in an interactive playback design. Our design allowed us to compare the performance of imitations from the following categories: (i) songs only experienced during the early tutoring; (ii) songs experienced both during early tutoring and interactive playbacks; and (iii) novel songs experienced only during the simulated interactions. In their second year, birds imitated song types from each category, including those from categories (i) and (ii) which they had failed to imitate before. In addition, the performance of these song types was different (category (ii) > category (i)) and more pronounced than for category (iii) songs. Our results demonstrate 'silent' song storage in nightingales and point to a graded influence of the time and the social context of experience on subsequent vocal imitation.