Vocal learning, the substrate for human language, is a rare trait found to date in only three distantly related groups of birds (parrots, hummingbirds, and songbirds) and four distantly related groups of mammals (humans, bats, cetaceans, and elephants). Brain pathways for vocal learning have been studied in the three bird groups and in humans, and they have a number of similarities. In addition, use of learned vocalizations is also similar among vocal learners. Together this suggests common selection pressures. Here I present hypotheses on what could have selected for or against vocal learning and associated brain pathways in birds and mammals. The brain pathways I suggest were selected from a pre-existing motor pathway. Selection for vocal learning behavior I suggest occurred by two factors: mating preference for varied vocalizations and a need for rapid adaptation to propagate sound in different environments. Selection against vocal learning I suggest occurred by predation, where varied vocalizations makes an animal an easier target for predators. Once predator selection pressure is overcome, then, I suggest, learned vocalizations can be used for other functions, such as abstract communication.
We review recent studies that examine the temporal resolution of the avian auditory system as measured behaviorally in a small songbird, the Zebra Finch (Taeniopygia guttata). These birds naturally learn and produce complex harmonic vocalizations. Here we created complex harmonic stimuli that simulate the fine temporal properties of these natural calls in order to probe the possible parallels between productive precision and perceptual acuity. The studies we review show that these birds are exquisitely sensitive to changes in temporal fine structure in complex sounds, 3–5 times more sensitive than humans, and probably other mammals. This sensitivity also was obtained with several types of synthetic harmonic stimuli that mimicked particular properties of natural signals, including harmonic sounds with individually altered components, Schroeder-phase complexes that control for envelope cues, and synthetic signals constructed from repeated single periods of natural calls. These last studies confirm that Zebra Finches are capable of discriminating among their species-specific vocalizations using only changes in temporal fine structure—something humans, tested on the same stimuli, cannot do.
The males of songbirds, parrots and hummingbirds develop complex song through learning. Males of some species mimic the vocalizations of other species and make their song more complex through vocal mimicry. Females of several songbird species respond preferentially to more complex song. The sensory exploitation hypothesis is an explanation how female preferences for complex song historically came to exist in birds. Female response to song readily habituates to repeated presentation of simple (that is, monotonous) song, while complex song can reduce habituation in female response to song. Males singing complex song might have exploited such preexisting property (or bias) in the female's response to song. This explanation is supported by experiments involving measurement of the expression of immediate early genes (IEGs). Analysis of IEG expression has been useful to reveal brain activation patterns associated with specific sensory stimuli. When exposed to male song, female songbirds and parrots show increased IEG expression in the auditory system in the caudal telencephalon, notably the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). Current data from female brains suggest that the NCM is related to song complexity. In addition, both of the NCM and the CMM may be involved in discriminating conspecific from heterospecific vocalizations.
Protein kinase C (PKC) is a key enzyme for neural plasticity. Our recent studies in Zebra Finches (Taeniopygia guttata) and Bengalese Finches (Lonchura striata var. domestica) strongly suggested to us that PKC is closely related to the plasticity for the song learning and alteration. In the present study, we examined the distribution of the isoforms of PKC in the male Zebra Finch brain, with an especial focus on the song control nuclei, using antibodies against the classical PKC isoforms (PKCα, β1, βII and γ). We determined the differential intracellular, cellular and regional distributions of the PKC isoforms in the avian brain. These comparisons of the distributions of the PKC isoforms give us further insights into the molecular mechanisms of avian song learning and maintenance.
In songbirds, the auditory neurons of the telencephalic song control nuclei, especially those in the high vocal center (HVC), respond to the bird's own song (BOS) selectively. Since songs are elicited by the sight of conspecific females and interrupted by intense visual stimulation, such as strobe lights, visual input might modulate this auditory selectivity. This study used acute electrophysiological experiments using Bengalese Finches (Lonchura striata var. domestica) to examine whether strobe lights affect this auditory response. The results showed that visual inputs did not affect the neural activities in response to the BOS. When the visual stimulus was presented alone, we did not record comparable neural activities to auditory stimuli, although vague, weak electrical potential fluctuations were observed. This means that direct visual inputs do not reach all HVC neurons that have BOS selectivity, and the effects of visual information might be very limited in the song control system. Although visual information should have some relationship to singing behaviors, such effects might be mediated by indirect connections from the visual system via unidentified emotional modules.
Bengalese Finches Lonchura striata var. domestica are extremely sexually dimorphic in their singing behavior; males sing complex songs, whereas females do not sing at all. The brain nuclei that control song in males are many times larger than those in females are, except the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), which comprises the same volume in both sexes. In this study, we examined the connectivity of the LMAN in female Bengalese Finches using a biotinylated dextran amine (BDA) in vivo tracing technique. We found that efferent connections of the female LMAN projected mainly to the robust nucleus of the arcopallium (RA), although the RA in female Bengalese Finches is much smaller than in males. Our data demonstrate that non-singing female Bengalese Finches possess projections connecting a song learning region to a song motor region. These connections may have functional roles in song perception.
Both auditory and visual signals are important to elicit avian courtship behaviour. The analysis of such signals has recently been strongly facilitated by the use of video and audio techniques. It has already been shown that male Zebra Finches (Taeniopygia guttata) show preferences to video images of conspecifics compared with heterospecifics and emit directed song towards live pictures of conspecific females. There is no experiment as yet to show whether Zebra Finches can also recognize intraspecific cues from videos, for example discriminate their mate from an unknown conspecific male or female. Zebra Finches were trained to choose between two live images from two video cameras, which were alternatively displayed on a 100 Hz CRT monitor by hopping on one or the other of two perches within the experimental cage. Our results show that most Zebra Finches are able to solve this task after one day of learning, the preference for one of the video images rising steadily. The birds easily distinguish between the live picture of a Zebra Finch of the opposite sex and an empty cage. The choice between an unknown female and an unknown male was more difficult, but was also learned by males and females. In another experiment, Zebra Finches had to choose between an unknown Zebra Finch female and their own mate. All males preferred the unknown female over their mate. An additional experiment indicated that the choice of the males is dependent mostly on visual, not auditory cues. In contrast, females mostly preferred their mate, and their choice was affected by manipulation of auditory cues.
We investigated the process of pair formation in Zebra Finches. Two males and two females, unfamiliar with each other, were put in a flight cage and we observed these four birds for 30 min each day for 10 days. In total, five sets of four birds were used. During the observation period, the position of each individual was recorded every minute. The occurrences of songs, agonistic behavior, and other behaviors were recorded in real time and additional video analyses were performed off line. On introducing the birds, the males immediately began fighting and a firm dominance hierarchy was established, usually within a few minutes. Most of the directed songs occurred during the first day and gradually the proportion of undirected songs increased. In each set, birds formed at least one intimate heterosexual pair. We analyzed the properties of the individuals that formed the pair. The results indicated that the heavier females pair-bonded quicker, and the males that won dominance bonded sooner and four out of five dominant males weighed more than the other male in each set. By contrast, the song duration and song quality of each male did not differ between the paired male and the other male. In our experimental setting, females did not pay as much attention to the song as to the social dominance. Therefore, the functional significance of courtship songs appears after the dominance hierarchy is established among males and is used as a secondary cue for mate choice in females.
A birdsong involves multiple traits that may have evolved under sexual selection pressure. There are two types of song traits: performance-related and elaboration-related traits. These two aspects of songs are partially independent, reflecting neural development and physical condition, respectively, but some song traits might interact with each other because they share the same mechanism for song production. Understanding the evolution of multiple ornaments requires knowledge of correlations among ornaments in the same individual. We explored the potential relationships between the following five song measures. We measured song duration and note rate as performance-related traits; and average note types, linearity index score, and entropy as elaboration-related traits for the analysis. First, we found a significant relationship between linearity and entropy, indicating that syntactical complexity was consistently measured in both different variables. However, note type repertoire was not significantly associated with the two measures of syntactical complexity. Different song nuclei are responsible for each aspect of hierarchically organized song structures. Specifically, a lower-order song nucleus (RA) codes note type, while higher-order song nuclei (HVC and Nif) program transition patterns. Considering that female Bengalese Finches prefer syntactically complex songs, sexual selection, especially female choice, has played a role in shaping brains; however, the sexual selection pressure for each song nucleus may differ in its intensity. Our investigation also revealed that those birds having a larger repertoire of note types tended to sing at lower speeds and require longer song bouts to sing syntactically complex songs. Hence, these results indicate that there are trade-offs and correlations between distinct aspects of performance-related and elaboration-related traits.
Vocal learning in birds is limited by both genetic and environmental factors. Innately determined, species-specific ranges of song parameters restrict song structures; the actual parameter values are determined by environmental inputs during learning. This is also true for some call notes. Here, we investigated the characteristics of songs and distance calls in a hybrid Bengalese–Zebra Finch and Bengalese-fostered Zebra Finches. The Bengalese-fostered Zebra Finches learned a limited part of the song elements, whereas the hybrid learned most of the foster father's song. However, the hybrid could not learn the acoustic morphology of Bengalese distance calls as well as the fostered finches. The results suggest that the neural circuitry for song element repertoire and call acoustic morphology are independent and that hybridization and cross-fostering procedures are useful tools for investigating genetic and environmental factors in vocal learning.
The Bengalese Finch Lonchura striata var. domestica has highly complex songs with element sequences similar in syntactic structure to that of human language. Because young learn songs by comparing their auditory memory of their father’s songs to the auditory feedback of a self-generated song, it is important to understand the auditory neural representation of element sequences. We developed a spiking neural network model of the song-control nucleus HVC that changes the weight among connected neurons via spike-timing-dependent plasticity (STDP), a biologically plausible learning rule. In the model, the dynamics of neural population converged into a stable activity distribution after sufficient learning steps. The network activity differentiated element pairs included in the input sequence from those that were not. Linear input sequences had better fine response selectivity for typical pairs than random or syntax inputs. However, real HVC neurons of Bengalese Finch respond to a wider range of pair stimuli. Thus, the actual neural representation of Bengalese Finch may be more broadly distributed, possibly because of simple STDP and other additive parameters or components. From a theoretical viewpoint, one of the most reliable neural coding schemes, Cantor coding, is a distributed, sequential coding system using fractal properties. We hypothesize that Bengalese Finch learn their complex song element sequences via Cantor coding.
Evolutionary biologists have paid much attention to studies of parasite-host interactions. The prevalence of blood parasites is highly dependent on diagnostic methods, season, and regions. Recently, polymerase chain reaction (PCR) based molecular diagnostic methods have been developed to detect the infection of blood parasites. In order to reevaluate the prevalence of blood parasites in Japanese passerines, I compared the prevalence of blood parasites found by microscopic examination with that found by PCR-based molecular diagnostics. 14.5% of individuals (225 of 1553) were infected with avian malaria, and 25.1% of individuals (220 of 878) were infected with avian trypanosome in Japan. The present study showed significantly higher prevalence of trypanosomes than previously reported. The trypanosome might represent a suitable agent for studying host-parasite interactions in birds, because it affects both growth and fitness. PCR-based molecular diagnostics revealed a higher prevalence of both avian malaria and trypanosome in the present study than in previous ones. The PCR-based molecular diagnostic method is more effective than microscopic examination for screening for infection of blood parasites, if the primes of a target parasite are available.
We studied the diel activity patterns of presence and absence from a heronry and post-breeding roosts of ten free-living Black-crowned Night Herons Nycticorax nycticorax in Honshu, Japan. We described their diel activity patterns and examined whether the patterns of individual herons varied while living in a heronry, and whether those patterns changed as the individual lived in the heronry or in a post-breeding roost. Six tagged herons were frequently absent from their heronries during the daytime. There were four distinctive types among the observed diel activity patterns: 1) absence of individual herons observed every other day, 2) presence at the heronry occurred largely after sunrise and before sunset, 3) individuals made many short foraging trips and short visits to the heronry throughout both the day and night, 4) absent only at night (nocturnal) and individuals left the roosting place exactly at sunset every day. The six herons that were absent from the heronry during the daytime varied their diel activity patterns while living in the heronry: for example, an individual switched from type 3 diel activity, to type 2. Three of the six herons were observed to move from a heronry to a post-breeding roost, and were found to change their behavioural pattern from being absent from the heronry during the daytime, to being absent only at night prior to, or at the time of, the move.
I studied the relationships between bird community and vegetation in Bavi National Park, Vietnam, during August and September 2004. Bird species richness and bird species diversity were correlated to physiognomic variables of the tree layer, in particular canopy closure and tree basal area. Shrub layer characteristics and floristics, expressed here as tree species richness and tree species diversity, were less correlated to bird species richness and diversity.
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