Perception of distance calls by budgerigars (Melopsittacus undulatus) and zebra finches (Poephila guttata): assessing species-specific advantages

Budgerigars (Melopsittacus undulatus) and zebra finches (Poephila guttata) share a common functional class of vocalizations called distance calls. The perception of species-specific distance calls by both species was measured with a habituation-dishabituation operant paradigm. Changes in discrimination performance were noted as listening conditions were modified or stimulus properties were altered. Both species showed better performance for calls of their own species. For zebra finches this tendency increased slightly when a background noise was added to the testing environment. Shifting the frequency region of the calls affected the discrimination performance of male budgerigars but not females or zebra finches. Reversing the temporal order of the calls affected the perceptual advantage for conspecific vocalizations in zebra finches but not in budgerigars. These results highlight species differences in perceiving acoustic communication signals.     

Selective auditory grouping by zebra finches: testing the iambic–trochaic law

Humans have a strong tendency to spontaneously group visual or auditory stimuli together in larger patterns. One of these perceptual grouping biases is formulated as the iambic/trochaic law, where humans group successive tones alternating in pitch and intensity as trochees (high–low and loud–soft) and alternating in duration as iambs (short–long). The grouping of alternations in pitch and intensity into trochees is a human universal and is also present in one non-human animal species, rats. The perceptual grouping of sounds alternating in duration seems to be affected by native language in humans and has so far not been found among animals. In the current study, we explore to which extent these perceptual biases are present in a songbird, the zebra finch. Zebra finches were trained to discriminate between short strings of pure tones organized as iambs and as trochees. One group received tones that alternated in pitch, a second group heard tones alternating in duration, and for a third group, tones alternated in intensity. Those zebra finches that showed sustained correct discrimination were next tested with longer, ambiguous strings of alternating sounds. The zebra finches in the pitch condition categorized ambiguous strings of alternating tones as trochees, similar to humans. However, most of the zebra finches in the duration and intensity condition did not learn to discriminate between training stimuli organized as iambs and trochees. This study shows that the perceptual bias to group tones alternating in pitch as trochees is not specific to humans and rats, but may be more widespread among animals.     

Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches (Taeniopygia guttata)

Zebra finches communicate via several distinct vocalizations, of which song is the most studied. Behavioral observations indicate that adults are able to discriminate among the songs of different conspecific individuals. In the wild, zebra finches live in structured but mobile colonies, and encounter new individuals on a frequent basis. Thus it seems plausible that adult finches might have the capacity to recognize and remember new songs they encounter on a single day, but this has never been directly tested. Here we devised a simple observational assay to determine whether adult male zebra finches show recognition of a song they have heard repeatedly from taped playbacks, over a single three hour period the day before. We quantified the rate of production of six discrete behaviors (short calls, contact calls, singing, short hops, long hops, and beak swipes) made by adult male zebra finches as they listened to the playbacks. At the onset of song playback, all birds suspended these behaviors and sat silently-occasionally moving their heads. Then, after a measurable period ("response latency"), the birds resumed these activities. We observed that the response latency was long (approximately 10 min) when birds were hearing a particular song for the first time. The response latency was much shorter (approximately 1-2 min) when the birds had heard the same song the day before. Thus, functional song memories must result from as little as 3 h of passive song-exposure. These results suggest that ongoing song learning may play a natural role in the daily life of adult zebra finches, and provide a behavioral reference point for studies of molecular and physiological plasticity in the adult auditory system.     

Perception of warble song in budgerigars (Melopsittacus undulatus): evidence for special processing

The long, rambling warble song of male budgerigars is composed of a large number of acoustically complex elements uttered in streams lasting minutes a time and accompanied by various courtship behaviors. Warble song has no obvious sequential structure or patterned repetition of elements, raising questions as to which aspects of it are perceptually salient, whether budgerigars can detect changes in natural warble streams, and to what extent these capabilities are species-specific. Using operant conditioning and a psychophysical paradigm, we examined the sensitivity of budgerigars, canaries, and zebra finches to changes in long (>6?min) natural warble sequences of a male budgerigar. All three species could detect a single insertion of pure tones, zebra finch song syllables, budgerigar contact calls, or warble elements from another budgerigar’s warble. In each case, budgerigars were more sensitive to these changes than were canaries or finches. When warble elements from the ongoing warble stream were used as targets and inserted, out of order, into the natural warble stream so that the only cue available was the violation of the natural ordering of warble elements, only budgerigars performed above chance. When the experiment was repeated with all the ongoing warble stream elements presented in random order, the performance of budgerigars fell to chance. These results show species-specific advantages in budgerigars for detecting acoustic changes in natural warble sequences and indicate at least a limited sensitivity to sequential rules governing the structure of their species-specific warble songs.     

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.     

Left-side dominance for song discrimination in Bengalese finches (Lonchura striata var. domestica)

Male Bengalese finches are left-side dominant for the motor control of song in the sensorimotor nucleus (the high vocal center, or HVc) of the telencephalon. We examined whether perceptual discrimination of songs might also be lateralized in this species. Twelve male Bengalese finches were trained by operant conditioning to discriminate between a Bengalese finch song and a zebra finch song. Before training, the left HVc was lesioned in four birds and the right HVc was lesioned in four other birds. The remaining four birds were used as controls without surgery. Birds with a left HVc lesion required significantly more time to learn to discriminate between the two songs than did birds with a right HVc lesion or intact control birds. These results suggest that the left HVc is not only dominant for the motor control of song, but also for the perceptual discrimination of song. Accepted after revision: 11 September 2001 Electronic Publication     

Significance of visual cues in choice behavior in the female zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis><Emphasis Type="Italic">castanotis</Emphasis>)

Female zebra finches show a preference for male zebra finches over heterospecific males based solely on the auditory cues of males, such as songs. The present study was designed to investigate whether females show a similar preference for male zebra finches based solely on visual cues. Using a Y-maze apparatus, social preference of female zebra finches was studied between male zebra finches and male Bengalese finches in three experiments. In experiment 1, where female zebra finches could see and hear live male zebra finches and male Bengalese finches, the females preferred to associate with the male zebra finches. In experiment 2, using a sound-attenuated experimental apparatus, subjects could see, but not hear, male zebra finches and male Bengalese finches. The subjects did not show a significant preference for associating with zebra finches. In experiment 3, as in experiment 2, females could see live male zebra finches and male Bengalese finches in the sound-attenuated chambers. However, in experiment 3, the subjects also heard prerecorded auditory cues (i.e., songs and calls) of male zebra finches, which were presented simultaneously in both arms of the maze. Although the females could not use the auditory cues to identify the location of the male zebra finches, they preferred to associate with the male zebra finches rather than the male Bengalese finches. These results suggest that visual cues alone were effective in initiating choice behaviors by females and that auditory cues facilitate such visually based choice behaviors. Electronic Publication     

Effect of acoustic cue modifications on evoked vocal response to calls in zebra finches (Taeniopygia guttata)

Besides their song, which is usually a functionally well-defined communication signal with an elaborate acoustic structure, songbirds also produce a variety of shorter vocalizations named calls. While a considerable amount of work has focused on information coding in songs, little is known about how calls' acoustic structure supports communication processes. Because male and female zebra finches use calls during most of their interactions and answer to conspecific calls without visual contact, we aimed at identifying which calls' acoustic cues are necessary to elicit a vocal response. Using synthetic zebra finch calls, we examined evoked vocal response of male and female zebra finches to modified versions of the distance calls. Our results show that the vocal response of zebra finches to female calls requires the full harmonic structure of the call, whereas the frequency downsweep of male calls is necessary to evoke a vocal response. It is likely that both female and male calls require matching a similar frequency bandwidth to trigger a response in conspecific individuals.     

The precedence effect in three species of birds (Melopsittacus undulatus, Serinus canaria, and Taeniopygia guttata)

The perceived locations of paired auditory images, simulating direct sounds and their echoes, have been recently studied in budgerigars (Melopsittacus undulatus; M. L. Dent & R. J. Dooling, 2003a, 2003b). In this article, the authors extend those experiments to include measurements of the precedence effect using a discrimination paradigm in two additional bird species: canaries (Serinus canaria) and zebra finches (Taeniopygia guttata). Although time courses of summing localization, localization dominance, and echo thresholds were similar across all species, budgerigars had slightly higher overall levels of discrimination. The results from these experiments add further support that the precedence effect in birds is similar to that found in other animals and that the ability to suppress echoes that might degrade localization and auditory object perception may be a general property of the vertebrate auditory system.     

Relative salience of syllable structure and syllable order in zebra finch song

There is a rich history of behavioral and neurobiological research focused on the ‘syntax’ of birdsong as a model for human language and complex auditory perception. Zebra finches are one of the most widely studied songbird species in this area of investigation. As they produce song syllables in a fixed sequence, it is reasonable to assume that adult zebra finches are also sensitive to the order of syllables within their song; however, results from electrophysiological and behavioral studies provide somewhat mixed evidence on exactly how sensitive zebra finches are to syllable order as compared, say, to syllable structure. Here, we investigate how well adult zebra finches can discriminate changes in syllable order relative to changes in syllable structure in their natural song motifs. In addition, we identify a possible role for experience in enhancing sensitivity to syllable order. We found that both male and female adult zebra finches are surprisingly poor at discriminating changes to the order of syllables within their species-specific song motifs, but are extraordinarily good at discriminating changes to syllable structure (i.e., reversals) in specific syllables. Direct experience or familiarity with a song, either using the bird’s own song (BOS) or the song of a flock mate as the test stimulus, improved both male and female zebra finches’ sensitivity to syllable order. However, even with experience, birds remained much more sensitive to structural changes in syllables. These results help to clarify some of the ambiguities from the literature on the discriminability of changes in syllable order in zebra finches, provide potential insight on the ethological significance of zebra finch song features, and suggest new avenues of investigation in using zebra finches as animal models for sequential sound processing.     

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.     

Absolute pitch: frequency-range discriminations in pigeons (Columba livia): comparisons with zebra finches (Taeniopygia guttata) and humans (Homo sapiens)

Absolute pitch (AP) is the ability to classify individual pitches without an external referent. The authors compared results from pigeons (Columba livia, a nonsongbird species) with results (R. Weisman, M. Njegovan, C. Sturdy, L. Phillmore, J. Coyle, & D. Mewhort, 1998) from zebra finches (Taeniopygia guttata, a songbird species) and humans (Homo sapiens) in AP tests that required classification of contiguous tones into 3 or 8 frequency ranges on the basis of correlations between the tones in each frequency range and reward. Pigeons' 3-range discriminations were similar in accuracy to those of zebra finches and humans. In the more challenging 8-range task, pigeons, like zebra finches, discriminated shifts from reward to nonreward from range to range across all 8 ranges, whereas humans discriminated only the 1st and last ranges. Taken together with previous research, the present experiments suggest that birds may have more accurate AP than mammals.     

Song perception during the sensitive period of song learning in zebra finches (Taeniopygia guttata)

The sensitive period is a special time for auditory learning in songbirds. However, little is known about perception and discrimination of song during this period of development. The authors used a go/no-go operant task to compare discrimination of conspecific song from reversed song in juvenile and adult zebra finches (Taeniopygia guttata), and to test for possible developmental changes in perception of syllable structure and syllable syntax. In Experiment 1, there were no age or sex differences in the ability to learn the discrimination, and the birds discriminated the forward from reversed song primarily on the basis of local syllable structure. Similar results were found in Experiment 2 with juvenile birds reared in isolation from song. Experiment 3 found that juvenile zebra finches could discriminate songs on the basis of syllable order alone, although this discrimination was more difficult than one based on syllable structure. The results reveal well-developed song discrimination and song perception in juvenile zebra finches, even in birds with little experience with song.     

Rule learning by zebra finches in an artificial grammar learning task: which rule?

A hallmark of the human language faculty is the use of syntactic rules. The natural vocalizations of animals are syntactically simple, but several studies indicate that animals can detect and discriminate more complex structures in acoustic stimuli. However, how they discriminate such structures is often not clear. Using an artificial grammar learning paradigm, zebra finches were tested in a Go/No-go experiment for their ability to distinguish structurally different three-element sound sequences. In Experiment 1, zebra finches learned to discriminate ABA and BAB from ABB, AAB, BBA, and ABB sequences. Tests with probe sounds consisting of four elements suggested that the discrimination was based on attending to the presence or absence of repeated A- and B-elements. One bird generalized the discrimination to a new element type. In Experiment 2, we continued the training by adding four-element songs following a ‘first and last identical versus different’ rule that could not be solved by attending to repetitions. Only two out of five birds learned the overall discrimination. Testing with novel probes demonstrated that discrimination was not based on using the ‘first and last identical’ rule, but on attending to the presence or absence of the individual training stimuli. The two birds differed in the strategies used. Our results thus demonstrate only a limited degree of abstract rule learning but highlight the need for extensive and critical probe testing to examine the rules that animals (and humans) use to solve artificial grammar learning tasks. They also underline that rule learning strategies may differ between individuals.     

Zebra finches and Dutch adults exhibit the same cue weighting bias in vowel perception

Vocal tract resonances, called formants, are the most important parameters in human speech production and perception. They encode linguistic meaning and have been shown to be perceived by a wide range of species. Songbirds are also sensitive to different formant patterns in human speech. They can categorize words differing only in their vowels based on the formant patterns independent of speaker identity in a way comparable to humans. These results indicate that speech perception mechanisms are more similar between songbirds and humans than realized before. One of the major questions regarding formant perception concerns the weighting of different formants in the speech signal (“acoustic cue weighting”) and whether this process is unique to humans. Using an operant Go/NoGo design, we trained zebra finches to discriminate syllables, whose vowels differed in their first three formants. When subsequently tested with novel vowels, similar in either their first formant or their second and third formants to the familiar vowels, similarity in the higher formants was weighted much more strongly than similarity in the lower formant. Thus, zebra finches indeed exhibit a cue weighting bias. Interestingly, we also found that Dutch speakers when tested with the same paradigm exhibit the same cue weighting bias. This, together with earlier findings, supports the hypothesis that human speech evolution might have exploited general properties of the vertebrate auditory system.     

Perception of mistuned harmonics in complex sounds by the bullfrog (Rana catesbeiana)

The ability of 73 male bullfrogs (Rana catesbeiana) to detect single mistuned harmonics in an otherwise periodic signal was studied. Bullfrogs in their natural environment were presented with playbacks of synthetic signals, resembling their species advertisement calls, that differed in the frequency of 1 harmonic component (out of 22). There were significant differences in the number and latency of the males' evoked vocal responses to these stimuli, suggesting that males were sensitive to the differences between the sounds. Differences in envelope shape (rate and depth of amplitude modulation) produced by the harmonic mistunings may underlie the differences in response. Frogs, like birds and humans, can discriminate sounds on the basis of harmonic structure, indicating that this is a general perceptual trait shared among vertebrates.     

Social learning of food types in zebra finches (<Emphasis Type="Italic">Taenopygia guttata</Emphasis>) is directed by demonstrator sex and feeding activity

In this study we examined how social learning of feeding preferences by zebra finches was affected by the identity of different demonstrators. We presented adult zebra finches with two demonstrators, one male and one female, that exhibited different food choices, and we recorded their subsequent preference when given a choice between the two food types. Previously it was found that young zebra finches' patterns of social learning are affected by the sex of the individual demonstrating a feeding behaviour. This result could be explained by the lack of exposure these animals had to the opposite sex, or by their mating status. Therefore, we investigated the social learning preferences of adult mated zebra finches. We found the same pattern of directed social learning of a different type of feeding behaviour (food colour): female zebra finches preferred the colour of food eaten by male demonstrators, whereas male zebra finches showed little evidence of any preference for the colour of food eaten by female demonstrators. Furthermore, we found that female observers' preferences were biased by demonstrators' relative feeding activity: the female demonstrator was only ever preferred if it ate less than its male counterpart. Electronic Publication     

Perceptual organization of acoustic stimuli by budgerigars (Melopsittacus undulatus): III. Contact calls

We trained budgerigars by operant conditioning to discriminate among a set of contact calls in a same-different task and analyzed response latencies from this task by using multidimensional-scaling (MDS) and cluster-analysis procedures. Humans listened to the same calls and indicated the similarity between pairs of calls by a direct rating procedure. An MDS program (sindscal) was used to arrange these complex acoustic stimuli in multidimensional space reflecting perceptual organization. Multiple regression techniques were used to identify the acoustic characteristics of contact calls that were correlated with the perceptual dimensions obtained from MDS. A number of spectral characteristics (e.g., peak frequency, rate of frequency modulation, and concentration of spectral energy) emerged as important for both budgerigars and humans, but the relative salience of these cues differed for the two species. Additional tests with two groups of budgerigars--cagemates and noncagemates--showed that experience with calls can change the salience of various acoustic characteristics used for perceptual organization and individual recognition.     

Comparing responses of four ungulate species to playbacks of baboon alarm calls

A growing body of evidence suggests that a wide range of animals can recognize and respond appropriately to calls produced by other species. Social learning has been implicated as a possible mechanism by which heterospecific call recognition might develop. To examine whether familiarity and/or shared vulnerability with the calling species might influence the ability of sympatric species to distinguish heterospecific alarm calls, we tested whether four ungulate species (impala: Aepyceros melampus; tsessebe: Damaliscus lunatus; zebra: Equus burchelli; wildebeest: Connochaetes taurinus) could distinguish baboon (Papio hamadryas ursinus) alarm calls from other loud baboon calls produced during intra-specific aggressive interactions (‘contest’ calls). Overall, subjects’ responses were stronger following playback of alarm calls than contest calls. Of the species tested, impala showed the strongest responses and the greatest difference in composite response scores, suggesting they were best able to differentiate call types. Compared with the other ungulate species, impala are the most frequent associates of baboons. Moreover, like baboons, they are susceptible to both lion and leopard attacks, whereas leopards rarely take the larger ungulates. Although it seems possible that high rates of association and/or shared vulnerability may influence impala’s greater ability to distinguish among baboon call types, our results point to a stronger influence of familiarity. Ours is the first study to compare such abilities among several community members with variable natural histories, and we discuss future experiments that would more systematically examine development of these skills in young ungulates.     

Frequency-range discriminations and absolute pitch in black-capped chickadees (Poecile atricapillus), mountain chickadees (Poecile gambeli), and zebra finches (Taeniopygia guttata)

The acoustic frequency ranges in birdsongs provide important absolute pitch cues for the recognition of conspecifics. Black-capped chickadees (Poecile atricapillus), mountain chickadees (Poecile gambeli), and zebra finches (Taeniopygia guttata) were trained to sort tones contiguous in frequency into 8 ranges on the basis of associations between response to the tones in each range and reward. All 3 species acquired accurate frequency-range discriminations, but zebra finches acquired the discrimination in fewer trials and to a higher standard than black-capped or mountain chickadees, which did not differ appreciably in the discrimination. Chickadees' relatively poorer accuracy was traced to poorer discrimination of tones in the higher frequency ranges. During transfer tests, the discrimination generalized to novel tones when the training tones were included, but not when they were omitted.