Effects of early song experience on song preferences and song control and auditory brain regions in female house finches (Carpodacus mexicanus)

We examined the effects of song tutoring on adult song preferences, volume of song-control brain regions, and activity of auditory brain regions in female house finches (Carpodacus mexicanus). Hand-reared females were tutored with local songs, foreign songs, or no song. We then examined adult song preferences, determined the Nissl-defined volume of the song-control nuclei HVc, Area X, and RA, and compared the number of cells immunoreactive for Zenk protein in the auditory regions NCM and cmHV, following playback of songs heard early in life (Tutor/Playback Match) versus not heard (Tutor/Playback Nonmatch). All hand-reared birds exhibited preferences for locally recorded song over foreign or heterospecific song. We found no difference in the volume of song-control nuclei among the three groups. As well, we found no difference in the number of Zenk immunoreactive cells in NCM and cmHV between females in the Tutor/Playback Match group and females in the Tutor/Playback Nonmatch group. Isolate-reared birds showed greater Zenk immunoreactivity following song playback than either tutored group. Thus, early auditory experience may not play a role in adult geographic song preferences, suggesting that genetic factors can lead to preferences for songs of local dialects. Song tutoring did not influence the size of song-control regions nor Zenk induction levels following song playback, suggesting that early experience with particular songs does not influence Zenk expression. However, overall greater activation in isolate females in auditory areas suggests that exposure to song early in life may increase the selectivity of Zenk activation to song playback in auditory areas.     

Male response to intruders is related to song characteristics in Darwin’s small tree finch (Camarhynchus parvulus)

Bird song functions in mate choice and species recognition, and hence variation in song can contribute to divergence and reproductive isolation. We used playback experiments to examine male response to conspecific song in Darwin’s small tree finch. Song is a reliable signal of bill morphology in this species, and individuals displayed stronger response to songs of males with similar bill size. These findings suggest that, in the context of territorial defence, males discriminate between intruders on the basis of song characteristics. Given that male response to song may be examined as a proxy for female response, this study also implies that females could discriminate between males on the basis of song. The findings suggest that: (1) perceived threat of intruders is related to reproductive competition and not fighting assessment, and (2) geographical isolation is not required for biologically meaningful song variation in Darwin’s finches.     

Acoustic characteristics, early experience, and endocrine status interact to modulate female zebra finches' behavioral responses to songs

Female songbirds use male songs as an important criterion for mate selection. Properties of male songs are thought to indicate the male's quality as a potential mate. Song preferences in female zebra finches are known to be influenced by two factors--early auditory experience and the acoustic characteristics of males' songs. Studies often investigate song preferences by priming females with estrogen. However, estrogenic influences on song preferences have not been studied. We investigated the relative influence of early auditory experience, acoustic features of songs, and estrogen availability on song responsiveness in female zebra finches. Juvenile female zebra finches were tutored for 10 days with 40 songs per day with one of three acoustically different song types--simple songs, long-bout songs or complex songs. A fourth group of females was untutored. Aside from this brief song exposure, females were raised and maintained without exposure to male songs. During adulthood, females' behavioral responses to the three song types were tested under three hormone conditions--untreated, estradiol-treated and 1,4,6-androstatriene-3,17-dione (ATD)-treated (to lower endogenous estrogen). Based on the results of our study, four conclusions can be drawn. First, song responsiveness in female zebra finches is strongly affected by minimal early acoustic experience. Second, inexperienced female zebra finches are inherently biased to respond more to complex songs over other song types Third, although female zebra finches are inherently biased to respond more to complex songs, early acoustic experience may either reinforce or weaken this inherent responsiveness to complex songs. Fourth, estrogen selectively accentuates song responsiveness in acoustically-experienced female zebra finches.     

Song preference of female Bengalese finches as measured by operant conditioning

Male songbirds approach females by using their songs. Knowing what females perceive and prefer in male songs is an important aspect of understanding courtship behavior. Male Bengalese finches (Lonchura striata var. domestica) sing complex sequence patterns with their own variety of elements. We tested female preference with phonologically different songs and sequentially different songs using an operant selection task. In the first experiment we presented the father’s song and an unfamiliar song that were phonologically different. Females clearly preferred the father’s song over a novel song. In the second experiment, we used the father’s song and its element order reversed song to test female preference for the difference in element sequence. In the third experiment, we presented different sequence complexity songs edited from the same unfamiliar song elements to test female preference for complex sequence. Females did not show a significant preference in either the second or third experiment. Results show that female Bengalese finches discriminated the difference in song elements, preferred familiar songs, and did not show preference for difference of sequence. This study did not support evidence that female Bengalese finches prefer a complex sequence. However, in future research, we should carefully investigate female preference for choosing mates in a natural context.     

Male House Finches with Elaborate Songs have Higher Reproductive Performance

The elaborate songs of male animals are thought to function in either territory defense (male–male communication) or mate attraction (male–female communication). In non‐territorial animals, male vocalizations are expected to function primarily in mate attraction, yet the reproductive consequences of male vocalizations in non‐territorial animals are poorly described. Here we explore the relationship between male song and male reproductive performance in a free‐living population of house finches, Carpodacus mexicanus, a non‐migratory, non‐territorial songbird. Based on recordings of 20 males, we analyzed three song features (song length, number of unique syllables per song, and song rate) and compared male song with two measures of within‐pair reproductive performance (nest initiation date and clutch size) and one measure of extra‐pair reproductive performance (whether males sired extra‐pair young). We demonstrate a positive association between male song and within‐pair reproductive performance; males that sang long songs initiated their first clutch significantly earlier and males that sang songs at a faster rate had larger clutches. Despite the fact that only one of our recorded males sired extra‐pair young in the nest of another male, this male's songs were the most elaborate for two of three song features measured, anecdotally suggesting that male song may play a role in both within‐pair and extra‐pair partner choice. These results suggest that male song is a sexually selected trait in non‐territorial house finches.     

Lack of premating isolation at the base of a phylogenetic tree

Darwin's finches in the Galápagos archipelago are an unusual example of adaptive radiation in that the basal split separates two lineages of warbler finches (Certhidea olivacea and Certhidea fusca) believed until recently to be only one species. The large genetic difference between them contrasts with their similarity in plumage, size, shape, and courtship behavior. They differ in song, which is a key factor in premating isolation of other sympatric Darwin's finches. We conducted playback experiments to see whether members of the population of C. olivacea on Santa Cruz Island would respond to songs of C. fusca from two islands, Genovesa and Pinta, and songs of C. olivacea from another island (Isabela). Another set of experiments was performed, using the same playback tapes, with C. fusca on Genovesa. Some members of both populations responded to all playbacks; therefore, the hypothesis of complete premating isolation on the basis of song is rejected. Discrimination between songs of the two lineages was inconsistent. We conclude that premating barriers to interbreeding among the tested populations have not arisen in the 1.5-2.0 m.yr. of their geographical isolation on different islands. This contrasts with strong premating barriers between more recently derived sympatric species. Early learning of song associated with morphology is later used in mate recognition. This explains why sympatric species that are vocally and morphologically distinct yet genetically less differentiated than Certhidea do not interbreed, whereas the Certhidea lineages that are genetically well differentiated but vocally and morphologically similar have no apparent premating barrier. We discuss this unusual situation in terms of the forces that have produced similarities and differences in song, morphology, and ecology and their relevance to phylogenetic and biological species concepts. Neither principles nor details are unique to Darwin's finches, and we conclude by pointing out strong parallels with some continental birds.     

The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings

Mate choice is among the most consequential decisions a sexually reproducing organism can make. In many songbird species, females make mate-choice decisions based, in part, on variation between males in songs that reflect their quality. Importantly, females may adjust their choice relative to the prevalence of high quality songs. In European starlings (Sturnus vulgaris), females prefer males that primarily sing long songs over those that primarily sing short songs, and sensitivity of the auditory telencephalon to song length depends on the prevalence of long songs in the environment. Several lines of evidence suggest a role for noradrenergic innervation of the auditory telencephalon in mediating this neuro- and behavioral plasticity. To simulate variation in quality of the song environment, we exposed adult female starlings to 1 week of either long or short songs and then quantified several monoamines and their metabolites in the caudomedial mesopallium and caudomedial nidopallium (NCM) using high performance liquid chromatography. We also used immunocytochemistry to assess these areas for immunoreactive dopamine-beta-hydroxylase (DBH-ir), the enzyme that synthesizes norepinephrine. We found that long songs elevated levels of the principal norepinephrine metabolite, the principal dopamine metabolite, and the probability of DBH-ir in the NCM compared to short songs. Song environment did not appear to influence norepinephrine or dopamine levels. Thus, the quality of the song environment regulates the local secretion of catecholamines, particularly norepinephrine, in the female auditory telencephalon. This may form a basis for plasticity in forebrain sensitivity and mate-choice behavior based on the prevalence of high-quality males.     

Early exposure leads to repeatable preferences for male song in female zebra finches

This study addressed the question of how early learning processes in females influence later preferences for a male trait. I tested whether exposure to song alone (of a male other than the father) was sufficient for inducing a stable (repeatable) preference in female zebra finches (Taeniopygia guttata) by limiting early exposure to tape tutoring. A group of controls heard no songs before also being tested in adulthood. Repeated tests for preferences for tutor or unfamiliar song were made, interspersed with additional tests involving new songs. Preferences were tested in an operant task where pecking of response keys led to song playback. Most females significantly preferred one of the two songs in a given test. In the first test, the relative preference for the tutor song was significantly higher for the tutored than for the control females. Subsequently, tutored females' preferences for the tutor song remained higher on average, but the two groups did not differ significantly. However, tutored, but not untutored females' preferences were highly repeatable between tests, suggesting that early exposure to song might lead to a consolidation ol choice behaviour, a previously unknown effect of early exposure to song in female songbirds.     

Male and female rufous‐and‐white wrens do not match song types with same‐sex rivals during simulated territorial intrusions

In birds with song repertoires, song‐type matching occurs when an individual responds to another individual's song by producing the same song type. Song‐type matching has been described in multiple bird species and a growing body of evidence suggests that song‐type matching may serve as a conventional signal of aggression, particularly in male birds in the temperate zone. Few studies have investigated song‐type matching in tropical birds or female birds, in spite of the fact that avian biodiversity is highest in the tropics, that female song is widespread in the tropics, and that female song is the ancestral state among songbirds. In this study of rufous‐and‐white wrens Thryophilus rufalbus, a resident neotropical songbird where both sexes sing, we presented territorial males and females with playback that simulated a territorial rival producing shared and unshared songs. In response, both males and females sang matched song types at levels statistically equal to levels expected by chance. Furthermore, males and females exhibited similar levels of aggression and similar vocal behaviours in response to playback of both shared and unshared songs. These results indicate that rufous‐and‐white wrens do not use song‐type matching in territorial conflicts as a conventional signal of aggression. We discuss alternative hypotheses for the function of song‐type sharing in tropical birds. In particular, we point out that shared songs may play an important role in intra‐pair communication, especially for birds where males and females combine their songs in vocal duets, and this may supersede the function of song‐type matching in some tropical birds.     

Song Perception in the Song Sparrow: Importance of Different Parts of the Song in Song Type Classification

Song sparrow (Melospiza melodia) males have repertoires of 6 to 12 song types, each song consisting of four or five contrasting phrases. Song types vary both within individuals (a singer varies successive renditions of a type within a singing bout) and between individuals (neighbors sing slightly different versions of a type), and in both cases this variation is concentrated in the later parts of the song. We speculated that type variation in the later parts of the song might be correlated with a perceptual tendency to classify song types primarily on the basis of the earlier parts of the song. We tested this hypothesis using a laboratory conditioning technique, supplemented by a field playback experiment. In the lab, song sparrows and white crowned sparrows were trained to discriminate between two distinct song types. In test sessions, they were presented with hybrid songs synthesized from varying proportions of the two training song types. For most birds and most song pairs, song classification was influenced by all parts of the song, with the beginning elements being most important. The field playback experiment used song type matching as the response measure. Each subject was presented a hybrid stimulus song consisting of the first half of one of his song types and the second half of another of his song types. Subjects replied with both ‘front matches’ and ‘back matches’ (60% were front matches).     

Adult bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax

Songbirds develop their songs by imitating songs of adults. For song learning to proceed normally, the bird's hearing must remain intact throughout the song development process. In many species, song learning takes place during one period early in life, and no more new song elements are learned thereafter. In these so-called close-ended learners, it has long been assumed that once song development is complete, audition is no longer necessary to maintain the motor patterns of full song. However, many of these close-ended learners maintain plasticity in overall song organization; the number and the sequence of song elements included in a song of an individual vary from one utterance to another, although no new song elements are added or lost in adulthood. It is conceivable that these species rely on continued auditory feedback to produce normal song syntax. The Bengalese finch is a close-ended learner that produces considerably variable songs as an adult. In the present study, we found that Bengalese finches require real-time auditory feedback for motor control even after song learning is complete; deafening adult finches resulted in development of abnormal song syntax in as little as 5 days. We also found that there was considerable individual variation in the degree of song deterioration after deafening. The neural mechanisms underlying adult song production in different species of songbirds may be more diverse than has been traditionally considered. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 343–356, 1997     

Female recognition of trills in the male calling song of the field cricket,<Emphasis Type="Italic"> Teleogryllus taiwanemma</Emphasis>

The calling song of the field cricket, Teleogryllus taiwanemma, is usually considered to consist of sequences of separate chirps. However, sometimes it comprises a phrase of several chirps in a row, with one long chirp (chirp) and a few short chirps (trills). In this study, I compared the phrase containing only chirps with that containing both chirps and trills by analyzing male songs and conducting playback experiments of male songs to females. The song analyses showed significant differences between chirps and trills for all song parameters except bandwidth. To test whether female preference differed with respect to the two phrases, I performed two-speaker playback experiments. When the same numbers of phrases were presented per unit time, females preferred the song with trills to that without trills. This result may reflect female preference for songs with greater sound density. In subsequent playback experiments, I equalized the total sound duration per unit time (duty cycle) in songs with and without trills. The numbers of females that preferred songs with and without trills did not differ significantly. This suggests that trills can attract females like chirps do, even though the two sounds have different components.     

The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

Juvenile male zebra finches develop their song by imitation. Females do not sing but are attracted to males' songs. With functional magnetic resonance imaging and event‐related potentials we tested how early auditory experience shapes responses in the auditory forebrain of the adult bird. Adult male birds kept in isolation over the sensitive period for song learning showed no consistency in auditory responses to conspecific songs, calls, and syllables. Thirty seconds of song playback each day over development, which is sufficient to induce song imitation, was also sufficient to shape stimulus‐specific responses. Strikingly, adult females kept in isolation over development showed responses similar to those of males that were exposed to songs. We suggest that early auditory experience with songs may be required to tune perception toward conspecific songs in males, whereas in females song selectivity develops even without prior exposure to song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2010     

Phonology and Geographic Song Discrimination in Song Sparrows

We investigated whether song sparrows discriminate foreign from local songs using specific phonologic markers, a mechanism of geographic discrimination previously described for some other songbirds. Song sparrows from Linesville, Pennsylvania (PA) respond more strongly to local songs than to songs from Millbrook, New York (NY). We identify 61 note categories in PA and NY songs, of which 13 are unique to PA, 17 are unique to NY, and 31 are shared. The most common note category in PA song, ‘buzz BO5’, is present in 89% of PA songs and only in 8% of NY songs; this difference in percentage representation is the largest we found for any note category. Substituting this potential PA marker into NY songs, however, did not make those songs more salient to PA sparrows; instead, PA males tested with territorial playback responded significantly less aggressively to NY/PA hybrid songs than to NY songs. A series of control experiments showed that song sparrows do not detect substitution of PA notes into PA songs or of NY notes into NY songs. The results weigh against the hypothesis that geographic discrimination in song sparrows is accomplished simply by recognition of a small number of phonologic markers.     

Tracing the development of learned song preferences in the female zebra finch brain with functional magnetic resonance imaging

In sexually dimorphic zebra finches (Taeniopygia guttata), only males learn to sing their father's song, whereas females learn to recognize the songs of their father or mate but cannot sing themselves. Memory of learned songs is behaviorally expressed in females by preferring familiar songs over unfamiliar ones. Auditory association regions such as the caudomedial mesopallium (CMM; or caudal mesopallium) have been shown to be key nodes in a network that supports preferences for learned songs in adult females. However, much less is known about how song preferences develop during the sensitive period of learning in juvenile female zebra finches. In this study, we used blood-oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to trace the development of a memory-based preference for the father's song in female zebra finches. Using BOLD fMRI, we found that only in adult female zebra finches with a preference for learned song over novel conspecific song, neural selectivity for the father's song was localized in the thalamus (dorsolateral nucleus of the medial thalamus; part of the anterior forebrain pathway, AFP) and in CMM. These brain regions also showed a selective response in juvenile female zebra finches, although activation was less prominent. These data reveal that neural responses in CMM, and perhaps also in the AFP, are shaped during development to support behavioral preferences for learned songs.     

Validating the female bioassay of cowbird song: Relating differences in song potency to mating success

Female cowbirds (Molothrus ater), maintained in isolation from males during the breeding season, respond to the playback of male song with copulatory postures. They respond more often to some songs than others. Song potency can thus be operationally defined by the number of copulatory responses a song elicits. The purpose of the present study was to validate this measure of song potency by investigating its relationship to mating success. We observed two colonies of cowbirds during the breeding season and recorded details of their courtship. In addition, song potency of the males was tested by playback with a different group of captive females. The results indicate a relationship between maximum song potency and mating success: the males that obtained the most copulations had songs of higher maximum potency and were also observed to have been more dominant during the winter and early spring.     

Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata

Brood-parasitic village indigobirds, Vidua chalybeata, were bred in captivity and foster-reared by their normal host species, the red-billed firefinch, Lagonosticta senegala, or by an experimental foster species, the Bengalese finch, Lonchura striata. Captive-reared female indigobirds were tested as adults for mate choice and for host choice. In tests of mate choice, female indigobirds responded preferentially towards mimicry songs of male indigobirds that were similar to those of the females' own foster parents. Females reared by Bengalese finches responded to male songs that mimicked Bengalese finch song rather than to male songs that mimicked their normal host species, the firefinch. In tests of host choice, females reared by Bengalese finches laid in the nests of Bengalese finches, and females reared by firefinches laid in the nests of firefinches. Wild-caught females showed the same behaviours as captive-bred females reared by firefinches. A female indigobird's social companions (firefinch or Bengalese) following her independence of her foster parents had no effect on her sexual response to male mimicry song or her choice of a host species in brood parasitism. The results support the predictions of a model of imprinting-like behaviour development in which young indigobirds focus their attention on their foster parents, rather than a model of innate bias for songs and nests of their normal host species, or a null model of nonspecific brood parasitism and differential survival. The results provide experimental support for the recent origin of brood parasite-host associations and the significance of imprinting in speciation in these brood parasites. Copyright 2000 The Association for the Study of Animal Behaviour.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

Strophe Length in Spontaneous Songs Predicts Male Response to Playback in the Hoopoe Upupa epops

Hoopoe (Upupa epops, Coraciformes) males produce a very simple song during the breeding season in order to attract females and repel intruders. Strophes vary in length (i.e. number of elements) both within and between males, and previous studies have shown that this song cue is positively correlated with male condition and breeding success. In the present study we tested whether strophe length of males influences male behaviour during intra‐sexual contests, in a colour‐ringed population in southeast Spain. Paired males were presented with a recorded song with long strophes during the pre‐laying period, while they were near their mates, in order to provoke male mate‐defence behaviour. Most males responded to the playback, but the strategy of defence adopted depended on their own strophe length in spontaneous songs recorded before the experiments. While singing responses were common to most of the males, only those using long strophes adopted the most risky strategy of approaching the loudspeaker. However, the males that approached produced abnormal songs during playback, that were shorter and with fewer strophes than those of males that did not approach, and used shorter strophes in comparison with spontaneous songs before the experiment. These differences in quality of the song produced in response to the playback suggest that long‐strophe males were basing their response mainly on attacking rather than singing, while short‐strophe males tried to resolve the contest at a distance by means of their song. These results show that strophe length reflects some component of the competitive ability of males (either physical strength or aggressiveness) in the hoopoe, which together with previous results regarding its role for female choice, show that it is a sexual signal with dual function.     

Broad Selectivity for Courtship Song in the Cricket Gryllus bimaculatus

Various characteristics of a long‐distance acoustic signal have been shown to vary to different degrees. It has been suggested that female preferences based on stable song parameters are stabilising or weakly directional, and preferences based on variable parameters are strongly directional. We tested this hypothesis based on a short‐distance signal (courtship song) produced by the field cricket, Gryllus bimaculatus. We studied the degree of variability of different courtship song parameters and the behavioural importance of several parameters using synthesised song models in playback experiments. We found that most of the courtship song elements of G. bimaculatus were quite variable (coefficient of variation, CV, in the range of 20–53%). The most variable parameter of the courtship song was the relative amplitude of two elements: high‐amplitude ticks and low‐amplitude pulses. Because songs containing only ticks (of rare occurrence) appeared to be more effective than songs with both ticks and pulses (of frequent occurrence), we consider female preferences to be directional. Alteration of less variable traits, such as the carrier frequency and duration of ticks (CV = 20–25%), had a different effect on female responsiveness. The synthesised songs with different carrier frequencies of ticks were as attractive to females as the positive control (courtship of muted males accompanied by playback of the recorded song). Altering the duration of ticks had a crucial effect on the female response rate, decreasing female responsiveness to the level observed in the negative control (courtship of muted males). Thus, we did not find a strong relationship between the variability of individual song parameters and their potential importance in song recognition and the evaluation of male quality. The partial inconsistency of our results with the data of other authors may be due to different patterns of past and current selection on long‐distance and short‐distance acoustic signals.