Cultural niche construction of repertoire size and learning strategies in songbirds

Birdsong is a complex cultural and biological system, and the selective forces driving evolutionary changes in aspects of song learning vary considerably among species. The extent to which repertoire size, the number of syllables or song types sung by a bird, is subject to sexual selection is unknown, and studies to date have provided inconsistent evidence. Here, we propose that selection pressure on the size and complexity of birdsong repertoires may facilitate the construction of a niche in which learning, sexual selection, and song-based homophily may co-evolve. We show, using a review of the birdsong literature and mathematical modeling, that learning mode (open-ended or closed-ended learning) is correlated with the size of birdsong repertoires. Underpinning this correlation may be a form of cultural niche construction in which a costly biological trait (for example, open-ended learning) can spread in a population (or be lost) as a result of direct selection on an associated cultural trait (for example, song repertoire size).     

Heavy metal pollution affects dawn singing behaviour in a small passerine bird

Although several studies have suggested that behavioural measures may be more comprehensive than other biomarkers for indicating an organism’s health or welfare, this has rarely been investigated in free-living terrestrial vertebrates. Here we examine the expression of dawn singing behaviour in a free-living small songbird in relation to environmental pollution. We compared the singing behaviour of male great tits Parus major inhabiting an area extremely polluted with heavy metals with that of males inhabiting areas of low(er) pollution (at 4 and 20 km distance from the pollution source). Males at the most polluted site had a significantly smaller repertoire size than males at the two other sites. They also produced a significantly lower total amount of song during the dawn chorus than the males at a distance of 4 km from the pollution source. Our results, although non-experimental and obtained in field conditions, strongly suggest that heavy metal pollution might affect the expression of singing behaviour. Taking into account that previous studies were not able to detect clear, straightforward differences between the health of great tits at the most polluted site and at 4 km distance from the pollution source, our results suggest that the singing behaviour of great tits may be a useful indicator of environmental stress at the population level.     

Re-expression of songs deleted during vocal development in white-crowned sparrows, Zonotrichia leucophrys

White-crowned sparrows learn and produce multiple song types as juveniles, but most individuals stop singing all except one by the end of the first singing season. This single song type is generally maintained throughout adulthood. We demonstrate that, at the start of the second and subsequent singing seasons, this species can recall songs that had been deleted during the first singing season. The re-expression of song occurred in both the oriantha and the gambelii subspecies. Although all our males recrystallized the original song in the second year, our results indicate a mechanism for seasonal song change without new song memorization. The traditional dichotomy of closed-ended versus open-ended learning is inadequate for birds that learn early in life but can change their song output seasonally. We suggest that species can exhibit a closed sensitive period for song memorization and first production, with the ability to recall deleted songs later in life. This type of learning, selective attrition followed by subsequent re-expression, may be used by some species currently considered open-ended learners. Copyright 2000 The Association for the Study of Animal Behaviour.     

Territory tenure in song sparrows is related to song sharing with neighbours, but not to repertoire size

Song repertoires may be a product of sexual selection and several studies have reported correlations of repertoire size and reproductive success in male songbirds. This hypothesis and the reported correlations, however, are not sufficient to explain the observation that most species have small song repertoire sizes (usually fewer than 10, often fewer than five song types). We examined a second important aspect of a male's song repertoire, the extent to which he shares songs with his neighbours. Song sharing has not been measured in previous studies and it may be partially confounded with repertoire size. We hypothesized that in song sparrows, Melospiza melodia, song sharing rather than repertoire size per se is crucial for male territorial success. Our longitudinal study of 45 song sparrows followed from their first year on territory showed that the number of songs a bird shares with his neighbourhood group is a better predictor of lifetime territory tenure than is his repertoire size. We also found that song sharing increases with repertoire size up to but not beyond eight to nine song types, which are the most common repertoire sizes in the population (range in our sample 5-13). This partial confound of song sharing and repertoire size may account for some earlier findings of territory tenure-repertoire size correlations in this species and other species having small- or medium-sized repertoires. Copyright 2000 The Association for the Study of Animal Behaviour.     

Vocal Plasticity – are Pied Flycatchers,Ficedula Hypoleuca,Open‐Ended Learners?

In some songbird species, large song repertoires are advantageous in female attraction, whereas song sharing with neighbours may give an advantage in male–male competition. Open‐ended learners, with the ability to memorize new song elements throughout their lives, may learn from territorial neighbours and thus benefit from increasing both repertoire size and song sharing. A distinction needs to be made between true adult song learning, i.e. memorization of novel song elements, and vocal plasticity resulting in changes in the use of previously memorized elements, such as the use of hidden repertoires or increased production of previously rare syllable types. We assessed the ability of adult pied flycatcher Ficedula hypoleuca males to learn previously unheard song elements and to change their song production in response to playback of unfamiliar, conspecific song, emulating a singing neighbour. After a 1‐week playback treatment, three out of 20 subjects had learned foreign song elements, providing evidence from the wild that pied flycatchers are true open‐ended learners. However, the syllable sharing with the playback stimulus repertoires had not changed, and the males’ repertoires had decreased rather than increased. Hence, we did not find support for increased syllable sharing with neighbours or increased repertoire size as functions of adult song learning in pied flycatchers. Because pied flycatcher song seems to serve mainly for mate attraction, copying of attractive syllable types is a possible alternative function of adult song learning in this species.     

Song learning in domesticated canaries in a restricted acoustic environment

Many songbirds learn their songs early in life from a song model. In the absence of such a model, they develop an improvised song that often lacks the species-typical song structure. Open-ended learners, such as the domesticated canary, are able to modify their songs in adulthood, although the mechanisms that guide and time the song-learning process are still not fully understood. In a previous study, we showed that male domesticated canaries lacking an adult song model in their first year substantially change their song repertoire and composition when exposed to normally reared conspecifics in their second year. Here, we investigate song development in descendants of canaries that were raised and kept as a peer group without a song model. Such males represent tutors with abnormal song characteristics. Interestingly, the F₁ generation developed quite normal song structure, and when brought into an environment with normally raised canaries in their second year, they did not modify their songs substantially. These results suggest that contact with an adult song model early in life is crucial for song crystallization, but also that song development is at least partly guided by innate rules. They also question the existing classification of canaries as open-ended learners.     

Limited Inter‐Annual Song Variation in the Serin (Serinus serinus)

Patterns of song plasticity in passerine birds beyond the first year are poorly studied. In general, songbirds are divided into two categories: open‐ended learners and closed‐ended learners, depending on the pattern of age‐related vocal plasticity. However, recent work based on longitudinal studies revealed a broader range of flexibility of song changes in adulthood. Serins sing very complex songs with large repertoires which are delivered in a very rigid way with little structural modification. However, there is little information on how serin song changes with age. We studied vocal plasticity in wild adult serins by recording male song over 2 years. The analyses show that male songs have only limited variation between years, with no increase in repertoire size and relatively small changes in their structural characteristics. Syllable production was very consistent within and between years with very little structural variation. New syllables represented only 8% of the repertoire, and they appeared to emerge from fusion or splitting of pre‐existing syllables. We conclude that serin song while structurally complex has a very limited age‐related plasticity after the first year. We hypothesise that this structural stability is a consequence of selection for performance consistency.     

Song and brain development in canaries raised under different conditions of acoustic and social isolation over two years

Early isolation experiments indicate that male songbirds learn their songs during an early sensitive period, although later work has shown that some open-ended learners modify songs in later years. Recent isolation experiments suggest that in some species song has a stronger genetic basis than previously thought. This study raised domestic canaries under different combinations of acoustic and social isolation and followed song development into the second year. Males raised alone in acoustic isolation developed songs with normal syllables, but larger repertoires and also produced syllables with lower repetition rates when compared to controls. The smallest repertoire occurred in males raised in a peer group. Isolate males had a smaller song control nucleus HVC than controls, but there was no effect on nucleus RA or on brain weight in general. In the second year, after introduction into a large normal colony, isolate and peer group males adjusted their syllable repertoire to normal size. In particular, the isolates reduced their repertoire even though the size of HVC showed a significant increase in volume. However, songs of isolate and peer group males still differ in repetition rate and number of single syllables in the common aviary. In contrast, control males showed low syllable turnover and no significant change in repertoire size. Nor did they show any significant change in the volumes of song control nuclei. It seems that complete isolation affects only some aspects of song and brain development, and later socialization corrects some but not all of these in the second year.     

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning.

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open-ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age-limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [3H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open-ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive.     

First-Year Common Nightingales (Luscinia megarhynchos) Have Smaller Song-Type Repertoire Sizes Than Older Males

Based on the assumptions that birdsong indicates male quality and that quality is related to age, one might expect older birds to signal their age. That is, in addition to actual body condition, at least some song features should vary with age, presumably towards more complexity. We investigated this issue by comparing repertoire sizes of free‐ranging common nightingale males in their first breeding season with those of older males. Nightingales are a good model species as they are open‐ended learners, where song acquisition is not confined to an early sensitive period of learning. Moreover, nightingales develop an extraordinarily large song‐type repertoire (approx. 180 different song types per male), and differences in repertoire size among males are pronounced. We analysed repertoire characteristics of the nocturnal song of nine nightingales in their first breeding season and compared them with the songs of nine older males. The repertoire size of older males was on average 53% larger than that of yearlings. When analysing two song categories of nightingales, whistle and non‐whistle songs separately, we found similar results. Our findings show marked differences in repertoire size between age categories, suggesting that this song feature may reflect a male's age. We discuss those mechanisms that may constrain the development of larger repertoires in first‐year males. Whether repertoire sizes are crucial for female mate choice or in vocal interactions among conspecific males remains open to further investigations.     

Adult Song Sparrows do not Alter their Song Repertoires

To understand fully the function of vocal learning, it is important to know when, during an individual's lifetime, learning occurs. Songbirds are generally categorized into two groups with respect to their adult song learning ability. 'Open-ended' song learners are able to learn to produce new songs in adulthood, whereas 'age-limited' song learners can only acquire songs during their first year of life. Researchers have long assumed that certain oscine species are open-ended or age-limited song learners, but the evidence to date has been inadequate to test these assumptions for most species. We tested the hypothesis that song sparrows ( Melospiza melodia ) are age-limited song learners who do not alter their song repertoires in adulthood by examining the song repertoires of 24 color-banded males who were fully recorded in two, three or four different years. We compared sonagrams of the song types produced by males in different years and looked for any changes in repertoire composition (i.e. added or dropped song types). With few exceptions, males produced song repertoires that were identical in every year they were recorded. The exceptions (four males who did not produce one of their song types during one recording session) were all cases in which we believe that we missed recording a song type that a male did indeed have, not that the males dropped a song type. The finding that adult males do not alter the composition of their song repertoires provides strong evidence that song sparrows are age-limited song learners. Although it is possible that song sparrows make subtle within-song type changes across years, such changes would not necessarily constitute new song learning.     

Social learning in birds and its role in shaping a foraging niche

We briefly review the literature on social learning in birds, concluding that strong evidence exists mainly for predator recognition, song, mate choice and foraging. The mechanism of local enhancement may be more important than imitation for birds learning to forage, but the former mechanism may be sufficient for faithful transmission depending on the ecological circumstances. To date, most insights have been gained from birds in captivity. We present a study of social learning of foraging in two passerine birds in the wild, where we cross-fostered eggs between nests of blue tits, Cyanistes caeruleus and great tits, Parus major. Early learning causes a shift in the foraging sites used by the tits in the direction of the foster species. The shift in foraging niches was consistent across seasons, as showed by an analysis of prey items, and the effect lasted for life. The fact that young birds learn from their foster parents, and use this experience later when subsequently feeding their own offspring, suggests that foraging behaviour can be culturally transmitted over generations in the wild. It may therefore have both ecological and evolutionary consequences, some of which are discussed.     

Species‐level repertoire size predicts a correlation between individual song elaboration and reproductive success

Birdsong has long been considered a sexually selected trait that relays honest information about male quality, and laboratory studies generally suggest that female songbirds prefer larger repertoires. However, analysis of field studies across species surprisingly revealed a weak correlation between song elaboration and reproductive success, and it remains unknown why only certain species show this correlation in nature. Taken together, these studies suggest that females in numerous species can detect and prefer larger repertoires in a laboratory setting, but larger individual repertoires correlate with reproductive success only in a subset of these species. This prompts the question: Do the species that show a stronger correlation between reproductive success and larger individual repertoires in nature have anything in common? In this study, we test whether between‐species differences in two song‐related variables—species average syllable repertoire size and adult song stability over time—can be used to predict the importance of individual song elaboration in reproductive success within a species. Our cross‐species meta‐analysis of field studies revealed that species with larger average syllable repertoire sizes exhibited a stronger correlation between individual elaboration and reproductive success than species with smaller syllable repertoires. Song stability versus plasticity in adulthood provided little predictive power on its own, suggesting that the putative correlation between repertoire size and age in open‐ended learners does not explain the association between song elaboration and reproductive success.     

Song Trait Similarity in Great Tits Varies with Social Structure

For many animals, long-range signalling is essential to maintain contact with conspecifics. In territorial species, individuals often have to balance signalling towards unfamiliar potential competitors (to solely broadcast territory ownership) with signalling towards familiar immediate neighbours (to also maintain so-called “dear enemy” relations). Hence, to understand how signals evolve due to these multilevel relationships, it is important to understand how general signal traits vary in relation to the overall social environment. For many territorial songbirds dawn is a key signalling period, with several neighbouring individuals singing simultaneously without immediate conflict. In this study we tested whether sharing a territory boundary, rather than spatial proximity, is related to similarity in dawn song traits between territorial great tits (Parus major) in a wild personality-typed population. We collected a large dataset of automatized dawn song recordings from 72 unique male great tits, during the fertile period of their mate, and compared specific song traits between neighbours and non-neighbours. We show here that both song rate and start time of dawn song were repeatable song traits. Moreover, neighbours were significantly more dissimilar in song rate compared to non-neighbours, while there was no effect of proximity on song rate similarity. Additionally, similarity in start time of dawn song was unrelated to sharing a territory boundary, but birds were significantly more similar in start time of dawn song when they were breeding in close proximity of each other. We suggest that the dissimilarity in dawn song rate between neighbours is either the result of neighbouring great tits actively avoiding similar song rates to possibly prevent interference, or a passive consequence of territory settlement preferences relative to the types of neighbours. Neighbourhood structuring is therefore likely to be a relevant selection pressure shaping variation in territorial birdsong.     

Song matching in the great tit Parus major L.

Great tits respond to playback of song from their own repertoire by singing the same song type as that on the tape. This is referred to as song matching. There is a good correlation between the probability of matching and response strength as indicated by latency, approach to the speaker and total number of songs. We propose that matching functions as a graded signal in territorial disputes.     

Syllable repertoire and the size of the song control system in captive canaries (Serinus canaria)

In songbirds, there is considerable interest in relationships between song structure and the size of the song control system in the forebrain. In male canaries, earlier studies have reported that repertoire size increased with age, and positive correlations were obtained between repertoire size and the volume of song control nuclei such as high vocal center (HVC). Here we investigate whether age has an effect upon both the song structure and the morphology of two song control nuclei [HVC and robustus archistriatalis (RA)] that are important in song production. We recorded songs from an aviary population of 1- and 2-year-old male domesticated canaries. We found that repertoire size, number of sexually attractive (sexy) syllables, and size of song nuclei did not differ between 1- and 2-year-old males. Neither did we find significant correlations between syllable repertoire size and the size of the song control nuclei. However, HVC size was positively correlated with the proportion of sexy syllables in the repertoires of 2-year-old males. Some older males may enhance vocal performance by modifying the control of syllables rather than by increasing repertoire size or neural space.     

Great tits responding to territorial intrusions sing less but alarm more on colder days

Bird song transmits information required to defend territories and attract mates. These functions contribute to fitness by affecting survival and reproductive success. Singing is also costly due to physiological costs. We used observational data to evaluate support for the hypothesis that lower temperatures result in decreased singing behaviour in wild great tits due to increased energy consumption during cold conditions required for thermoregulation. More than 6,500 simulated territorial intrusions were performed over an 8-year period in twelve nest box populations of great tits Parus major south of Munich, Germany. We measured song rate as well as the number of alarm calls and the aggressive response of territorial males to a simulated territorial intrusion. We found a decrease in song rate with decreasing current temperature, but also a concurrent increase in the number of alarm calls. Night temperature did not affect these acoustic traits. We conclude that warmer conditions allow birds to choose more energetically expensive (yet functionally superior) activities during territorial intrusions, thereby facilitating avoidance of physical aggressiveness during territorial intrusions.     

Singing Activity Reveals Personality Traits in Great Tits

In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well‐studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.     

Comparative analyses of song complexity and song-control nuclei in fourteen oscine species

Most studies on the relationship between measures of song behavior and the sizes of song control nuclei have focused on one or two oscine species, and often show inconsistent results. To address this issue, we first measured four variables for song complexity, i.e., song repertoire size, syllable repertoire size, the mean number of syllables per phrase (MNS) and the number of syllables in the longest phrase (NSLP), and the sizes of three song control nuclei, i.e., HVC, RA (the robust nucleus of the arcopallium), and Area X in 14 oscine species from eight families. To tackle the problem of statistical non-independence that probably existed among the closely related species, we reconstructed the phylogeny of the species studied using mitochondrial cytochrome b DNA sequences from GenBank. By using the methods adopted in most previous reports, we tested the relationship between song complexity and the sizes of the song control nuclei. We found that: 1) the absolute sizes of RA and Area X, but not of HVC, were positively correlated to the three measures of song complexity, but that only the residual size of RA in regard to telencephalon size was significantly correlated to the song measures; 2) independent contrasts analysis showed RA and Area X to be significantly associated with NSLP. Our results indicated that the relationship between song behavior and its neural structures varied among song nuclei, suggesting that each song control nucleus may play a different role in song behavior.     

Facultative Adjustment of Brood Sex Ratio in Response to Indirect Manipulation of Behaviour

Sex allocation theory states that parents should adjust their offspring sex ratio according to the expected fitness returns from sons and daughters. Several recent studies indicate that such adaptive manipulation of offspring sex ratio is achievable, and that it may be influenced by e.g. morphological characters. Here we manipulate behaviour through interspecific cross-fostering of great tits ( Parus major ) and blue tits ( Cyanistes caeruleus ), and investigate its effect on the offspring sex ratio of adults that were themselves cross-fostered as chicks. The experience of being raised by a different species has previously been shown to result in aberrant species assortative behaviour and song, and a lowered dominance status during winter. Brood sex ratios of conspecifically breeding pairs with and without cross-fostered members were compared. Broods with at least one cross-fostered parent contained significantly more males than did control broods. Sex of cross-fostered parents did not influence the brood sex ratio. We conclude that female great tits and blue tits seem to be able to adjust the sex ratio of their broods, and that changes in their own or their partners' behaviour may elicit such adjustments.