Hector Fabio Rivera-Gutierrez

Multiple signals for multiple messages: great tit, **Parus major**, song signals age and survival

Birdsong is a well-known sexually selected trait that plays a major role in female choice and male – male interactions. Although birdsong has been studied for many years, it has only recently been suggested that it is a multifaceted signal that could encompass multiple sexually selected traits. According to the theories on the evolution and maintenance of multiple sexually selected signals, the different components of birdsong may signal multiple, redundant or unreliable information on male quality. We used a cross-sectional approach to examine whether the expression of song in the great tit was differentially related to any of three measures of quality: age, condition and survival. We analysed several informative characteristics in great tit song concerning diversity, output, performance and consistency to see whether different traits were simultaneously related to the studied quality parameters, or if, in contrast, each song trait was related to only one of the measures of quality. Song consistency and repertoire size were strongly related to only one of the studied parameters (age and survival, respectively), indicating that different song traits signal specific quality characteristics, and providing, therefore, evidence to support the multiple-signal hypothesis. Moreover, measures of song performance and song output (phrase and strophe rate) correlated positively with repertoire size, which might indicate that, at the same time, great tit song is signalling redundant information. In addition, some song characteristics did not correlate with any of the quality parameters measured, suggesting that those song traits might provide unreliable information.

Tuning and fading voices in songbirds: age-dependent changes in two acoustic traits across the life span

Age-related phenotypic changes (maturation–senescence) commonly occur during an organism’s lifetime. While maturation is usually considered as a measure of individual quality, senescence is associated with loss of function and physiological deterioration. To date, little is known about age-dependent expression of acoustic sexually selected traits over a lifetime. Using a free-living population of great tits, Parus major, we recorded the song of individually marked males in a standardized way during a 4-year period, in a longitudinal design. The study focused on two previously identified, acoustic, sexually selected signals: song consistency and repertoire size. Young (1–2 years old) and old (5–6 years old) individuals expressed lower song consistency than individuals at intermediate age (3–4 years old), suggesting song tuning during the first 3 years of life, and deterioration after the peak is reached. Repertoire size, in contrast, did not vary with age. To the best of our knowledge, our study is the first to evaluate song changes at advanced age and to report senescence effects on song expression in free-living songbirds. Our results suggest that, similarly to speech in humans, different aspects of birdsong are differentially affected by age: while motor performance traits (song consistency) deteriorate with age, language skills (repertoire size) may not be affected during the life span.

Songs differing in consistency elicit differential aggressive response in territorial birds

Acoustic signals during intrasexual interactions may help receivers to establish the cost and benefits of engaging in a confrontation versus avoiding the cost of escalation. Although birdsong repertoires have been previously suggested as providing information during agonistic encounters, the cost (time/neural resources) of assessing large repertoires may decrease the efficiency of the signal for mutual assessment. Acoustic-structural features may, therefore, be used to enable a fast and accurate assessment during this kind of encounters. Recently, it has been suggested that the consistency of songs may play a key role during intrasexual interactions in bird species. Using a playback experiment in a colour-ringed great tit population, we tested the hypothesis that songs differing in consistency may elicit a differential response, indicating that the signal is salient for the receivers. Great tit males clearly responded more aggressively towards highly consistent songs. Our findings, together with previous evidence of increased song consistency with age in the great tit, suggest that song consistency provides information on experience or dominance in this species, and this phenomenon may be more widespread than currently acknowledged.

The Female Perspective of Personality in a Wild Songbird: Repeatable Aggressiveness Relates to Exploration Behaviour

Males often express traits that improve competitive ability, such as aggressiveness. Females also express such traits but our understanding about why is limited. Intraspecific aggression between females might be used to gain access to reproductive resources but simultaneously incurs costs in terms of energy and time available for reproductive activities, resulting in a trade-off. Although consistent individual differences in female behaviour (i.e. personality) like aggressiveness are likely to influence these reproductive trade-offs, little is known about the consistency of aggressiveness in females. To quantify aggression we presented a female decoy to free-living female great tits (Parus major) during the egg-laying period, and assessed whether they were consistent in their response towards this decoy. Moreover, we assessed whether female aggression related to consistent individual differences in exploration behaviour in a novel environment. We found that females consistently differed in aggressiveness, although first-year females were on average more aggressive than older females. Moreover, conform life history theory predictions, ‘fast’ exploring females were more aggressive towards the decoy than ‘slow’ exploring females. Given that personality traits are often heritable, and correlations between behaviours can constrain short term adaptive evolution, our findings highlight the importance of studying female aggression within a multivariate behavioural framework.

An experimental study on the causal relationships between (ecto-)parasites, testosterone and sexual signalling

Bird song is considered to have evolved via sexual selection and should as such honestly signal aspects of the quality of its bearer. To ensure honesty, the immunocompetence handicap hypothesis proposed a dual role of testosterone, having positive effects on sexual signalling but suppressive effects on immune function. However, recent studies showed that it is rather an immune activation that suppresses the androgen production. This reversed chain of causation may significantly alter the pathways, which translate the effects of parasites and pathogens into changes in the expression of male sexual traits. We infested male canaries with Ixodes ricinus tick nymphs to investigate the causal relationships between (ecto-)parasites, testosterone and sexual signalling, here singing behaviour. We focused on flexible song traits, which may quickly reflect changes in the infestation status, and tested whether these effects relate to changes in the plasma testosterone levels or health state. The experimental tick infestation altered the males’ song performance by reducing song consistency, a trait that had previously been identified to reflect male quality. The tick infestation lowered the plasma testosterone levels and had a negative effect on the health status in terms of a reduced hematocrit. Our pathway analysis then revealed that it is the parasite-induced reduction of the plasma testosterone levels but not of the health state that caused the changes in song consistency. Thus, our study supports the view that it is the effect of parasites and immune activation on plasma testosterone levels that generates the trade-off between immunocompetence and sexual signalling.

Are low-frequency songs sexually selected, and do they lose their potency in male–female interactions under noisy conditions?

We agree with Halfwerk et al. (1) on the importance of including the receivers when studying the impact of anthropogenic noise. However, we find the conclusion that the use of low-frequency song is sexually selected in great tits and that noisy conditions affect male–female communication premature for several reasons.

Songbirds never forget : long-lasting behavioural change triggered by a single playback event

Many behavioural studies rely on playback experiments. While it is known that songbirds decrease behavioural responses after short-term repeated stimulation, long-term behavioural changes due to playbacks are unknown. We studied the response to playbacks in a free-living songbird in the long-term, while also studying the repeatability of the behaviour. Locomotor behaviour (a proxy of aggressiveness) decreased one year after first exposure to a single playback. Song response, however, remained consistent, suggesting that these two behaviours may provide different information. Locomotor behaviour was less repeatable than the song response to playback, the latter showing significant between-years repeatability. To the best of our knowledge, our study is the first to report long-term decrease in response to playbacks in a songbird, and that some aspects of the response to playback are repeatable. Similar studies in other species or populations of the great tit are important, to examine the generality of our findings.

Simulation of the song motor pathway in birds: A single neuron initiates a chain of events that produces birdsong with realistic spectra properties

Birdsong is a complex learned behavior regulated by Neuromuscular coordination of different muscle sets necessary for producing relevant sounds. We developed a heterogeneous and stochastically connected neural network representing the pathway from the high vocal center (HVC) to the robust nucleus of the arcopallium (RA) neurons that drive the muscles to generate sounds. We show that a single active neuron is sufficient to initiate a chain of spiking events that results to excite the entire network system. The network could synthesize realistic bird sounds spectra, with spontaneous generation of intermittent sound bursts typical of birdsong (song syllables). This study confirms experiments on animals and on humans, where results have shown that single neurons are responsible for the activation of complex behavior or are associated with high-level perception events.

Learning speed is affected by personality and reproductive investment in a songbird

Individuals from different taxa, including songbirds, differ consistently in behaviour and personality when facing different situations. Although our understanding of animal behaviour has increased, knowledge about between-individual differences in cognitive abilities is still limited. By using an experimental approach and a free-living songbird (Parus major) as a model, we attempted to understand between-individual differences in habituation to playbacks (as a proxy of learning speed), by investigating the role of personality, age and reproductive investment (clutch size). Pre-breeding males were tested for exploration (a proxy of personality) in standardized conditions. In addition, the same individuals were exposed to three playbacks in the field during incubation. Birds significantly moved less, stayed further away and overlapped less the playback with successive playback stimulation. While a decrease in the locomotor behaviour can be explained by personality, differences in habituation of overlapping were predicted by both reproductive investment and personality. Fast explorers habituated less. Moreover, males paired to females with larger clutches did not vary the intensity of overlapping. Since habituation requires information for recognition of non-threatening signals, personality may bias information gathering. While fast explorers may collect less information from the environment, slow explorers (reactive birds) seem to pay attention to environmental clues and collect detailed information. We provided evidence that the rate of habituation of behavioural responses, a proxy of cognitive abilities, may be affected by different factors and in a complex way.