Cross-fostering diminishes song discrimination in zebra finches (Taeniopygia guttata)

Song-production, -discrimination, and -preferences in oscine birds are dually influenced by species identity and the ontogenetic environment. The cross-fostering of a model species for recognition research, the zebra finch (Taeniopygia guttata) into heterospecific nests of the Bengalese finch (Lonchura striata vars. domestica) allows an exploration of the sensory limits of early development and the effects of species-specific acoustic cues upon song discrimination in adulthood. To quantify the song preferences of female and male normal-reared (control) and Bengalese finch fostered zebra finches, we recorded multiple behavioral measures, including spatial proximity, vocalization rates and response latency, during sequential song-playback choice-trials using both tutor species’ songs and the songs of two other ecologically relevant Australian species, the owl finch (Taeniopygia bichenovii) and the star finch (Neochmia ruficauda). Response strength was variable between the different measures, but no differences were detected within the specific behavioral responses towards the song playbacks of the two sexes. Control subjects strongly preferred their own species’ songs while Bengalese-fostered zebra finches exhibited reduced song discrimination between con-, tutor-, and heterospecific songs. Overall behavioral responsiveness was also modulated by social ontogeny. These results indicate a difference in the strength of preference for song that is dependent on the species identity of the rearing environment in oscine birds and illustrate the role of multiple behavioral measures and ecologically relevant stimulus species selection in behavioral research using zebra finches.     

Discrimination of individual vocalizations by black-capped chickadees (Poecile atricapilla)

The auditory perceptual abilities of male black-capped chickadees (Poecile atricapilla) were examined using an operant go/no-go discrimination among 16 individual vocalizations recorded at 5 m. The birds learned to discriminate about equally well among eight male chickadee fee-bee songs and eight female zebra finch (Taeniopygia guttata) distance calls. These results do not indicate that chickadees have a species-specific advantage in individual recognition for conspecific over heterospecific vocalizations. We then transferred the chickadees to a discrimination of the same songs and calls rerecorded at a moderate distance. These results showed accurate transfer of discrimination from 16 vocalizations recorded at 5 m to novel versions of the same 16 songs and calls rerecorded at 25 m. That is, chickadees recognized individual songs and calls despite degradation produced by rerecording at 25 m. Identifying individual vocalizations despite their transformation by distance cues is here described as a biologically important example of perceptual constancy.     

Modes of perceiving and processing information in birdsong (Agelaius phoeniceus, Molothrus ater, and Homo sapiens)

In a previous study I examined the abilities of red-winged blackbirds and brown-headed cowbirds trained with a go-right/go-left procedure to identify conspecific and alien song themes (Sinnott, 1980). Results showed that each bird species exhibited superior identification of conspecific final "trill" or "whistle" elements, relative to the alien species. The present study extends these results by examining human perception of these same song stimuli, by examining the effects of tutoring birds with alien final song elements, and by using latency analyses to investigate processing modes that are not apparent from analyses of percent-correct scores. Results suggest three different processing modes: First, humans attend primarily to the final song elements. Second, birds identifying alien songs attend primarily to the introductory elements and disregard information in the final elements. Third, birds identifying conspecific songs process both the initial and final elements, but their response latencies indicate that they direct their attention primarily to the initial elements and process the final elements without investing more time than do the alien birds that fixate on the initial elements. Conspecific special processing is discussed in relation to various psychophysical, ethological, and psycholinguistic frameworks. Human perception of birdsong is discussed in relation to backward recognition masking.     

Amplitude modulation of sexy phrases is salient for song attractiveness in female canaries (Serinus canaria)

Song discrimination and recognition in songbird species have usually been studied by measuring responses to song playbacks. In female canaries, Serinus canaria, copulation solicitation displays (CSDs) are used as an index of female preferences, which are related to song recognition. Despite the fact that many studies underline the role of song syntax in this species, we observed that short segments of songs (a few seconds long) are enough for females to discriminate between conspecific and heterospecific songs, whereas such a short duration is not sufficient to identify the syntax rules. This suggests that other cues are salient for song recognition. In this experiment, we investigated the influence of amplitude modulation (AM) on the responses (CSDs) of female canaries to song playbacks. We used two groups of females: (1) raised in acoustic isolation and (2) raised in normal conditions. When adult, we tested their preferences for sexy phrases with different AMs. We broadcast three types of stimuli: (1) songs with natural canary AM, (2) songs with AM removed, or (3) song with wren Troglodytes troglodytes AM. Results indicate that female canaries prefer and have predispositions for a song type with the natural canary AM. Thus, this acoustic parameter is a salient cue for song attractiveness.     

Social metrics of song learning

Five metrics of song learning are described for brown-headed cowbirds (Molothrus ater). The intent of these metrics is to capture not only the behavior of the song learner but the social context in which song learning occurs. Playback procedures, observations of mating, and acoustic and functional assessment of song content are combined to yield measures of song potency, functional validity, social dynamics, vocal flexibility, and social reactivity. Taken as a whole, the results revealed by these metrics indicate that males learn to be effective singers by attending to the social consequences of their behavior.     

Lower begging responsiveness of host versus parasitic brown-headed cowbird (Molothrus ater) nestlings is related to species identity but not to early social experience

The survival of young brood parasites depends critically on their many adaptations to exploit hosts. Parasitic survival is particularly related to competitive superiorty for foster parental care whenever host young are not destroyed in parasitized nests.Brown-headed cowbirds (Molothrus ater) are generalist obligate parasites whose early social environments are unpredictable regarding host species and numbers of nestmates. Young avian brood parasites typically beg more intensively and loudly than foster siblings, but an untested prediction is that young parasites are also more likely to respond by begging to a wider variety of stimulus types. Avian vocalizations were used in a playback experiment to stimulate begging behavior in cowbird hosts. Compared with age-matched cowbird nestlings, hosts begged less frequently to acoustic stimuli, and lower begging responsiveness was irrespective of whether hosts had been reared in parasitized nests.     

Multiple levels of representation of song by European starlings (Sturnus vulgaris): open-ended categorization of starling song types and differential forgetting of song categories and exemplars

Four European starlings (Sturnus vulgaris) were trained to discriminate among conspecific and heterospecific song segments in a go/no-go operant task. In Experiment 1, the starlings discriminated among novel starling and heterospecific songs, indicating an open-ended category of conspecific song types. The starlings also showed excellent memory for reinforced conspecific songs and discriminated among subordinate categories of conspecific song. In Experiment 2, the starlings were presented with the song segments from Experiment 1 after an 8-month delay period. The starlings retained the discrimination between conspecific and heterospecific songs but not among conspecific songs. The starlings also retained memory for individual singers over the 8-month delay. Starlings categorize song at the level of species, and at subordinate categories of song types, and may have superior long-term retention of song categories relative to song exemplars.     

Self-referent phenotype matching in a brood parasite: the armpit effect in brown-headed cowbirds (Molothrus ater)

Most birds and mammals learn characteristics of conspecifics from their parents and siblings. In interspecific brood parasites, however, early social learning could lead to species recognition errors because young are reared among heterospecifics. Conceivably, juvenile parasites might inspect and memorize aspects of their own phenotype, and later match features of encountered individuals to that template. We tested for such self-referent phenotype matching by manipulating feather colors of hand-reared fledglings (n = 21) of the parasitic brown-headed cowbird (Molothrus ater). In simultaneous choice trials (n = 6 trials/subject) between dyed and normal-colored adult females, juvenile cowbirds (< 2 months old) approached more quickly and associated preferentially with individuals that were colored similar to themselves. These preferences remained even when differences between the associative behaviors of juvenile males and females were controlled statistically. Our data imply that cowbirds incorporate their own plumage color into their recognition template. This provides the first evidence of self-referent phenotype matching through experimental manipulation of a recognition cue. Received: 11 April 2000 / Accepted after revision: 2 September 2000     

Agonistic character displacement in social cognition of advertisement signals

Interspecific aggression between sibling species may enhance discrimination of competitors when recognition errors are costly, but proximate mechanisms mediating increased discriminative ability are unclear. We studied behavioral and neural mechanisms underlying responses to conspecific and heterospecific vocalizations in Alston’s singing mouse (Scotinomys teguina), a species in which males sing to repel rivals. We performed playback experiments using males in allopatry and sympatry with a dominant heterospecific (Scotinomys xerampelinus) and examined song-evoked induction of egr-1 in the auditory system to examine how neural tuning modulates species-specific responses. Heterospecific songs elicited stronger neural responses in sympatry than in allopatry, despite eliciting less singing in sympatry. Our results refute the traditional neuroethological concept of a matched filter and instead suggest expansion of sensory sensitivity to mediate competitor recognition in sympatry.     

Discrimination of acoustically similar conspecific and heterospecific vocalizations by black-capped chickadees (<Emphasis Type="Italic">Poecile atricapillus</Emphasis>)

Chickadees produce a multi-note chick-a-dee call in multiple socially relevant contexts. One component of this call is the D note, which is a low-frequency and acoustically complex note with a harmonic-like structure. In the current study, we tested black-capped chickadees on a between-category operant discrimination task using vocalizations with acoustic structures similar to black-capped chickadee D notes, but produced by various songbird species, in order to examine the role that phylogenetic distance plays in acoustic perception of vocal signals. We assessed the extent to which discrimination performance was influenced by the phylogenetic relatedness among the species producing the vocalizations and by the phylogenetic relatedness between the subjects’ species (black-capped chickadees) and the vocalizers’ species. We also conducted a bioacoustic analysis and discriminant function analysis in order to examine the acoustic similarities among the discrimination stimuli. A previous study has shown that neural activation in black-capped chickadee auditory and perceptual brain regions is similar following the presentation of these vocalization categories. However, we found that chickadees had difficulty discriminating between forward and reversed black-capped chickadee D notes, a result that directly corresponded to the bioacoustic analysis indicating that these stimulus categories were acoustically similar. In addition, our results suggest that the discrimination between vocalizations produced by two parid species (chestnut-backed chickadees and tufted titmice) is perceptually difficult for black-capped chickadees, a finding that is likely in part because these vocalizations contain acoustic similarities. Overall, our results provide evidence that black-capped chickadees’ perceptual abilities are influenced by both phylogenetic relatedness and acoustic structure.     

Counting Chicks Before They Hatch: Female Cowbirds Can Time Readiness of a Host Nest for Parasitism

ABSTRACT— Here we show that demands associated with brood parasitism have favored sophisticated cognitive abilities in female brown-headed cowbirds. We discovered that cowbirds can use the rate at which eggs are added to a nest across days to assess the readiness of the nest for incubation, which would allow them to synchronize laying with the host and avoid nests where incubation has most likely commenced. In three experiments, cowbirds investigated and laid eggs in artificial nests that differed in the number of eggs they contained. Across days, we added eggs to nests at different rates to simulate differences in the timing of reproduction of the hosts. Cowbirds avoided a nest if the number of eggs that had been added was less than the number of days that had elapsed. The ability of females to remember egg number and compare changes in egg number across days allows them to select nests most suitable for parasitism.     

A Brain of Her Own: A Neural Correlate of Song Assessment in a Female Songbird

The song control region in the avian forebrain is a series of discrete, interconnected nuclei mediating song learning and production. It has been studied in males or in species where both sexes sing. Little is known about the neural correlates of song perception in nonsinging females, often the intended recipients of song. We studied cowbirds (Molothrus ater), a species in which only males sing but in which females discriminate between males on the basis of song. We focused on nucleus lMAN because it has been implicated in early song acquisition, a stage relevant to both sexes to choose among competing acoustic models. We found that volume of lMAN was monomorphic in cowbirds. Moreover, the volume and neuronal number of female lMAN were positively correlated with selectivity of copulatory responding. The results provide strong evidence of nonsinging female's use of “song” control nuclei for song perception without the possibility of song production.     

Biological relevance of acoustic signal affects discrimination performance in a songbird

The fee-bee song of the black-capped chickadee (Poecile atricapillus) is a two-note, tonal song that can be sung at different absolute pitches within an individual. However, these two notes are produced at a consistent relative pitch. Moreover, dominant birds more reliably produce songs with this species-typical interval, compared to subordinate birds. Therefore, we asked whether presenting the species-typical relative pitch interval would aid chickadees in solving pitch interval discriminations. We found that species-typical relative pitch intervals selectively facilitated discrimination performance using synthetic sine-wave stimuli. Using shifted fee-bee song notes from recordings of naturally produced songs, birds learned the discrimination in fewer trials overall compared to synthetic stimuli. These results may reflect greater generalization among stimuli that occur outside species-typical production parameters. In addition, although sex differences in performance are rarely observed in acoustic discriminations in chickadees, female chickadees performed more accurately compared to males.     

Sexual differences in memory in shiny cowbirds

Avian brood parasites depend on other species, the hosts, to raise their offspring. During the breeding season, parasitic cowbirds (Molothrus sp.) search for potential host nests to which they return for laying a few days after first locating them. Parasitic cowbirds have a larger hippocampus/telencephalon volume than non-parasitic species; this volume is larger in the sex involved in nest searching (females) and it is also larger in the breeding than in the non-breeding season. In nature, female shiny cowbirds Molothrus bonariensis search for nests without the male’s assistance. Here we test whether, in association with these neuroanatomical and behavioural differences, shiny cowbirds display sexual differences in a memory task in the laboratory. We used a task consisting of finding food whose location was indicated either by the appearance or the location of a covering disk. Females learnt to retrieve food faster than males when food was associated with appearance cues, but we found no sexual differences when food was associated with a specific location. Our results are consistent with the view that parasitism and its neuroanatomical correlates affect performance in memory tasks, but the effects we found were not in the expected direction, emphasising that the nature of avian hippocampal function and its sexual differences are not yet understood. Received: 30 April 1998 / Accepted after revision: 5 September 1998     

Auditory scene analysis in estrildid finches (Taeniopygia guttata and Lonchura striata domestica): a species advantage for detection of conspecific song

Operant-conditioning techniques were used to investigate the ability of zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) to detect a zebra finch or a Bengalese finch target song intermixed with other birdsongs. Sixteen birds were trained to respond to the presence of a particular target song, either of their own species (n = 8) or of another species (n = 8). The birds were able to learn a discrimination between song mixtures that contained a target song and song mixtures that did not, and they were able to maintain their response to the target song when it was mixed with novel songs. Zebra finches, but not Bengalese finches, learned the discrimination with a conspecific target more quickly and were worse at detecting a Bengalese finch in the presence of a conspecific song. The results indicate that selective attention to birdsongs within an auditory scene is related to their biological relevance.     

Recognition of heterospecific alarm vocalizations by bonnet macaques (Macaca radiata)

Recognition of heterospecific alarm vocalizations is an essential component of antipredator behavior in several prey species. The authors examined the role of learning in the discrimination of heterospecific vocalizations by wild bonnet macaques (Macaca radiata) in southern India The bonnet macaques' flight and scanning responses to playbacks of their own alarm vocalizations were compared with their responses to playbacks of vocalizations of Nilgiri langurs (Trachypithecus johnii), Hanuman langurs (Semnopithecus entellus), and sambar deer (Cervus unicolor). The study was conducted in 3 regions that differed in the frequency with which bonnet macaques encountered these species and included an urban setting. Call recognition was highest in adults and in regions where individuals were frequently exposed to the calling species; calls were not recognized by urban monkeys. Thus, age and experience are important factors in heterospecific call recognition by bonnet macaques.     

Song copying by humpback whales: themes and variations

Male humpback whales (Megaptera novaeangliae) produce long, structured sequences of sound underwater, commonly called songs. Humpbacks progressively modify their songs over time in ways that suggest that individuals are copying song elements that they hear being used by other singers. Little is known about the factors that determine how whales learn from their auditory experiences. Song learning in birds is better understood and appears to be constrained by stable core attributes such as species-specific sound repertoires and song syntax. To clarify whether similar constraints exist for song learning by humpbacks, we analyzed changes over 14 years in the sounds used by humpback whales singing in Hawaiian waters. We found that although the properties of individual sounds within songs are quite variable over time, the overall distribution of certain acoustic features within the repertoire appears to be stable. In particular, our findings suggest that species-specific constraints on temporal features of song sounds determine song form, whereas spectral variability allows whales to flexibly adapt song elements.Electronic Supplementary Material Supplementary material is available for this article at .     

Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite

Brood parasitism imposes several fitness costs on the host species. To reduce these costs, hosts of avian brood parasites have evolved various defenses, of which egg rejection is the most prevalent. In the face of variable host-parasite mimicry and the costs of egg discrimination itself, many hosts reject only some foreign eggs. Here, we experimentally varied the recognition cues to study the underlying cognitive mechanisms used by the Chalk-browed Mockingbird (Mimus saturninus) to reject the white immaculate eggs laid by the parasitic Shiny Cowbird (Molothrus bonariensis). Immaculate eggs are the only parasite eggs rejected by this host, as it accepts all polymorphic, spotted eggs laid by cowbirds. Using a within-breeding pair experimental design, we tested for the salience of spotting, UV reflectance, and brightness in eliciting rejection. We found that the presence of spotting significantly decreased the probability of rejection while increments in brightness significantly increased rejection frequencies. The cognitive rules underlying mockingbird rejection behavior can be explained by a decision-making model which predicts changes in the levels of rejection in direct relation to the number of relevant attributes shared between host and parasite eggs.     

Behavioral consequences of song learning: Discrimination of song types by male white-crowned sparrows

The functional significance of learned population differences in male song in the white-crowned sparrow was explored in natural populations using playback tests. Laboratory results have shown that learning of the population-specific song seems to take place in early life and is strongly dependent upon the nature of the auditory experience at that time. However, the varied results of recent studies make it difficult to reach a confident conclusion about the ecological functions of song learning. The present research took advantage of naturally occurring variation in the differences between songs of adjacent populations to determine a function relating degree of difference in song to intensity of territorial singing elicited. Applying a typological evaluation of syllable structure to the four segments of the song allowed a crude quantitative ranking of the differences between local songs and playback stimuli. These results, together with those of other studies, suggest a unimodal aggressive response function of males to songs of other males. A maximum response to songs slightly different from the local song environment suggests that male exclusion based upon acquired song components may contribute to the maintenance of discrete and stable song dialects.     

Experience with songs in adulthood reduces song-induced gene expression in songbird auditory forebrain

Male songbirds learn to produce song within a limited phase early in life; however they continue to learn to recognize songs in adulthood. Studies looking at Zenk activation after exposure to songs learned early in life for song production and songs learned in adulthood show opposite patterns of activation, suggesting distinct neural mechanisms may be involved in these two forms of learning. In this study, we look at IEG Zenk activation in auditory regions NCM and CMM of song sparrows (Melospiza melodia) to see whether recent exposure to song in adulthood leads to greater or decreased Zenk activation upon hearing that song versus a novel song. We found significantly lower activation in birds exposed to previously heard songs versus novel songs in vNCM but not dNCM, though further analysis suggest an overall trend in NCM. We found no significant difference in the amount of activation to previously heard songs vs. novel songs in CMM. These results support previous findings suggesting that activation is reduced to learned stimuli; we discuss possible implications of these findings in relation to song production learning early in life and song recognition learning in adulthood.