Song Learning in Bengalese Finches: a Comparison with Zebra Finches

Male Bengalese finches, Lonchura striata var. domestica, learn their song from an adult male conspecific with whom they can interact at 35 to 70 days of age and normally-raised males fail to reproduce song which they have only heard before or after this time. Birds which have been raised by their mother alone and those which have been deprived of a song tutor during the learning phase produce abnormal songs with indistinct elements and little or no phrase structure; this is typical of males which fail to hear adult song during their development. These songs are unstable and are replaced by normal songs, if there is an opportunity to learn from an adult male conspecific. Presumably, this flexibility in the time when young males learn acts as a safeguard to ensure that normal conspecific song is produced. These results bear striking similarity to those on zebra finch song development. Differences between the two species, especially in the learning of call notes by female zebra finches, are discussed.     

Sexual Partner Preference in Female Zebra Finches: The Role of Early Hormones and Social Environment

This experiment investigated the effects of early estrogen treatment and sex composition of the social environment on sexual partner preference in female zebra finches, a pair-bonding socially monogamous species. Birds were injected daily with estradiol benzoate (EB) or the steroid vehicle for the first 2 weeks posthatch and then lived in either a unisex (all-female) or a mixed sex group from 40 to 100 days. After 100 days birds were implanted with testosterone propionate and given three kinds of tests: tests with a stimulus female, two-choice mate preference tests with male and female stimuli, and colony tests to assess pairing preference in a more naturalistic context. Both EB and unisex housing independently resulted in a preference for females (masculinized preference) in the two-choice tests, but only females with both EB treatment and unisex living were more likely to pair with females in the colony tests. Sexual partner preference, a key sexually dimorphic component of mate choice, appears to be organized by sex steroids in this pair-bonding species, but in a manner that may be mediated by the social environment.     

Early Developmental Conditions and Male Attractiveness in Zebra Finches

Traits used in mate choice are often costly to produce or maintain, and thus can reflect an individual’s current condition. Mate choice, however, might not only be influenced by the current condition of a potential partner, but also by the condition it had experienced during its early development which can have strong and long‐lasting effects on various traits. Here we studied the effects of different early developmental conditions, imposed by brood size manipulations (small, medium and large broods), on male attractiveness as measured by female choice experiments in zebra finches (Taeniopygia guttata). In three different experiments, we allowed females to choose between males that had been raised in different experimental brood sizes. In none of the experiments, females showed a significant preference for males which had experienced better developmental conditions, i.e. were raised in the relatively smaller experimental broods. Song rate was higher in males coming from small than large broods, but females did not prefer males that sang more. These results suggest that sexual attractiveness either was not affected by our experimental treatment or that males subsequently had compensated in their overall attractiveness for negative effects of early developmental conditions.     

Drinking Songs: Alcohol Effects on Learned Song of Zebra Finches

Speech impairment is one of the most intriguing and least understood effects of alcohol on cognitive function, largely due to the lack of data on alcohol effects on vocalizations in the context of an appropriate experimental model organism. Zebra finches, a representative songbird and a premier model for understanding the neurobiology of vocal production and learning, learn song in a manner analogous to how humans learn speech. Here we show that when allowed access, finches readily drink alcohol, increase their blood ethanol concentrations (BEC) significantly, and sing a song with altered acoustic structure. The most pronounced effects were decreased amplitude and increased entropy, the latter likely reflecting a disruption in the birds’ ability to maintain the spectral structure of song under alcohol. Furthermore, specific syllables, which have distinct acoustic structures, were differentially influenced by alcohol, likely reflecting a diversity in the neural mechanisms required for their production. Remarkably, these effects on vocalizations occurred without overt effects on general behavioral measures, and importantly, they occurred within a range of BEC that can be considered risky for humans. Our results suggest that the variable effects of alcohol on finch song reflect differential alcohol sensitivity of the brain circuitry elements that control different aspects of song production. They also point to finches as an informative model for understanding how alcohol affects the neuronal circuits that control the production of learned motor behaviors.     

Flavoprotein Autofluorescence Imaging of Visual System Activity in Zebra Finches and Mice

Large-scale brain activity patterns can be visualized by optical imaging of intrinsic signals (OIS) based on activity-dependent changes in the blood oxygenation level. Another method, flavoprotein autofluorescence imaging (AFI), exploits the mitochondrial flavoprotein autofluorescence, which is enhanced during neuronal activity. In birds, topographic mapping of visual space has been shown in the visual wulst, the avian homologue of the mammalian visual cortex by using OIS. We here applied the AFI method to visualize topographic maps in the visual wulst because with OIS, which depends on blood flow changes, blood vessel artifacts often obscure brain activity maps. We then compared both techniques quantitatively in zebra finches and in C57Bl/6J mice using the same setup and stimulation conditions. In addition to experiments with craniotomized animals, we also examined mice with intact skull (in zebra finches, intact skull imaging is not feasible probably due to the skull construction). In craniotomized animals, retinotopic maps were obtained by both methods in both species. Using AFI, artifacts caused by blood vessels were generally reduced, the magnitude of neuronal activity significantly higher and the retinotopic map quality better than that obtained by OIS in both zebra finches and mice. In contrast, our measurements in non-craniotomized mice did not reveal any quantitative differences between the two methods. Our results thus suggest that AFI is the method of choice for investigations of visual processing in zebra finches. In mice, however, if researchers decide to use the advantages of imaging through the intact skull, they will not be able to exploit the higher signals obtainable by the AFI-method.     

The Onset of Song Learning and Song Tutor Selection in Fledgling Zebra Finches

We investigated song development in the pre‐independent zebra finch (aged 15–35 d), a period when neural pathways for song learning and production are forming and social influences outside the family are limited. Expt 1 investigated the onset and the minimum duration of tutoring needed for song learning in fledglings. We found most begin to learn song from 25 d of age and need about 10 d contact with the father tutor to make accurate copies. This onset corresponds with major developments in the formation of the neural circuitry implicated in song acquisition. Subsong also begins on day 25 suggesting that the sensory and motor phases of song learning fully overlap in the zebra finch. Our findings support the hypothesis that the song circuitry is fully functional by 35 d of age and the sensitive phase for zebra finches extends therefore from about days 25–65. However, only the first 10 d of this period are necessary to learn a tutor's song with fair accuracy. Expt 2 investigated the role of the paternal bond, spatial proximity and mating status in a fledgling's choice of song tutor where the father was the sole parent. Young chose the father over single unrelated males (expt 2a) or unrelated males in company with their female partners (expt 2b). Given the close spatial proximity of both potential tutors to the fledglings it is probably the filial bond, established via paternal care that is the cause of this preference. Zebra finches sing the same song phrase in two contrasting contexts: female‐directed song during pre‐copulatory courtship and undirected song where no female or display is involved. In expt 3 we tested the song learning preference of pre‐independent young for two categories of non‐paternal tutors: those singing predominantly female‐directed song and those singing exclusively undirected song. There was a small, but significant, preference for fledgling zebra finches to copy songs from males that sang female‐directed song. This preference is consistent with the hypothesis that young males not only learn the acoustic features of their tutor's song but also the visual and dynamic movements that constitute the courtship display.     

斑胸草雀的鸣声学习

鸣声是鸟类重要的生物学特征和分类特征。由于生理结构和神经控制方面的差异,不同种群和同一种群的不同个体都有自己特有的鸣声特征,正是利用这些特征,鸟类才能在集群、取食、迁徙、喂雏、御敌和求偶等行为中进行通讯。作为一种能够利用语音信息进行交流的高等脊椎动物,斑胸草雀的鸣声特别是鸣啭能力获得,需要有一个适宜的学习对象,并在一段特定的时间内,经历复杂的学习过程才能实现。     

Female Social Feedback Reveals Non-imitative Mechanisms of Vocal Learning in Zebra Finches

1. Download high-res image (269KB)
2. Download full-size image

     

Facilitation and Dominance in a Schooling Predator: Foraging Behavior of Florida Pompano,Trachinotus carolinus

Presumably an individual’s risk of predation is reduced by group membership and this ‘safety in numbers’ concept has been readily applied to investigations of schooling prey; however, foraging in groups may also be beneficial. We tested the hypothesis that, when feeding in groups, foraging of a coastal fish (Florida Pompano, Trachinotus carolinus) on a benthic prey source would be facilitated (i.e. fish feeding in groups will consume more prey items). Although this question has been addressed for other fish species, it has not been previously addressed for Florida Pompano, a fish known to exhibit schooling behavior and that is used for aquaculture, where understanding the feeding ecology is important for healthy and efficient grow-out. In this experiment, juvenile Florida Pompano were offered a fixed number of coquina clams (Donax spp.) for one hour either in a group or as individuals. The following day they were tested in the opposite configuration. Fish in groups achieved greater consumption (average of 26 clams consumed by the entire group) than the individuals comprising the group (average of 14 clams consumed [sum of clams consumed by all individuals of the group]). Fish in groups also had fewer unsuccessful foraging attempts (2.75 compared to 4.75 hr^-1) and tended to have a shorter latency until the first feeding activity. Our results suggest fish in groups were more comfortable feeding and more successful in their feeding attempts. Interestingly, the consumption benefit of group foraging was not shared by all – not all fish within a group consumed equal numbers of clams. Taken together, the results support our hypothesis that foraging in a group provides facilitation, but the short-term benefits are not equally shared by all individuals.     

Sex-Specific Audience Effect in the Context of Mate Choice in Zebra Finches

Animals observing conspecifics during mate choice can gain additional information about potential mates. However, the presence of an observer, if detected by the observed individuals, can influence the nature of the behavior of the observed individuals, called audience effect. In zebra finches (Taeniopygia guttata castanotis), domesticated males show an audience effect during mate choice. However, whether male and female descendants of the wild form show an audience effect during mate choice is unknown. Therefore, we conducted an experiment where male and female focal birds could choose between two distinctive phenotypes of the opposite sex, an artificially adorned stimulus bird with a red feather on the forehead and an unadorned stimulus bird, two times consecutively, once without an audience and once with an audience bird (same sex as test bird). Males showed an audience effect when an audience male was present and spent more time with adorned and less time with unadorned females compared to when there was no audience present. The change in time spent with the respective stimulus females was positively correlated with the time that the audience male spent in front of its cage close to the focal male. Females showed no change in mate choice when an audience female was present, but their motivation to associate with both stimulus males decreased. In a control for mate-choice consistency there was no audience in either test. Here, both focal females and focal males chose consistently without a change in choosing motivation. Our results showed that there is an audience effect on mate choice in zebra finches and that the response to a same-sex audience was sex-specific.     

Constraints on the Evolution of Reciprocity: An Experimental Test with Zebra Finches

Reciprocity is apparently uncommon in animal societies because it requires, to evolve, specialized cognitive abilities that most species would not possess. In particular, memory would be important because cooperation can emerge and be maintained only if the same opponents interact repeatedly and adjust their decisions to their opponent’s previous move. To investigate how these constraints influence reciprocity, we first conducted a preliminary foraging experiment with zebra finches (Taeniapygia guttata) to insure that corticosterone elevations impaired the birds’ event memory capabilities. Then, we performed a reciprocity experiment with established pairs that were tested in a two‐choice apparatus under two different conditions: once with an empty implant and once with an implant of corticosterone. We found that the birds were capable of sustained cooperation in the Prisoner’s Dilemma treatment but only when they had an empty implant. Thus, our results support the hypothesis that limitations in event memory constraint the frequency of reciprocity and hence would make this form of cooperation difficult for non‐human animals. In addition, as levels of stress hormones can differ greatly among individuals, our findings might also contribute explaining individual variation in the propensity to cooperate.     

Survivorship, dispersal and sex ratios of Zebra Finches Taeniopygia guttata in southeast Australia

Membership of three permanent breeding colonies of Zebra Finches Taeniopygia guttata studied in farmland changed continually due to arrival and departure of birds from distant colonies. Sixty-six percent of adults stayed for less than 1 month, and many that stayed longer disappeared for extended periods. Over 78% of adults captured were hatched in other colonies and only 23% made a breeding attempt in their natal colony. There was no sex-biased natal dispersal or philopatry, but there were sex differences in the timing of dispersal. Sex ratios at the end of parental care were variable and may depend on food resources. Adult ratios were slightly male-biased. Annual losses of adults ranged from 72 to 82% across colonies, but mortalities and dispersal were heavily confounded by high adult mobility. The oldest bird was more than 5 years old. A total of 67% of young were lost between fledging and nutritional independence at 35 days of age, and only 20% of fledglings survived to day 80, the age of first breeding. Artificial supplies of seed at baited walk-in traps prolonged the stay of dispersing adults from other colonies, enhanced the survivorship of young hatched in the colony and possibly affected the secondary sex ratio. In this southeast part of their Australia-wide distribution, Zebra Finch populations appear to be highly mobile over a very large home range with extensive free interchange of members among a number of permanent breeding colonies. High mobility may be adaptive for exploiting patches of seed and water in a highly erratic environment.     

Tissue mass dynamics during egg-production in female Zebra Finches Taeniopygia guttata: dietary and hormonal manipulations

Changes in tissue masses associated with egg production were investigated in female Zebra Finches Taeniopygia gutatta using dietary and hormonal manipulations. We tested three hypotheses: that changes in organ masses, (a) reflect utilisation of endogenous nutrient stores due to inadequate daily dietary intake, (b) involve changes in organ structure or 'functional capacity', and (c) are initiated by onset of reproductive development (e.g. elevated plasma estrogen or yolk precursor levels, oviduct growth). Pectoral muscle lean dry mass was 18–22% lower in breeding females at the 1-egg stage compared to non-breeders, and this was independent of nutritional plane, i.e. similar changes occurred in birds provided with supplemental protein or egg food. Heart lean dry mass was also lower (16%) in breeding females, but only in birds on a low-quality seed diet, not in birds on supplemented diets. Decreases in total liver mass (14%) were due to changes in lipid content not lean dry mass, and were diet-dependent. These results demonstrate that changes in organ masses associated with egg production are complex, and do not simply reflect a general mobilisation of stored protein. We discuss why there is no hypertrophy of biosynthetic or metabolic 'machinery' associated with egg production in birds (cf. reproducing mammals). Exogenous 17β-estradiol induced plasma levels of yolk precursors typical of breeding birds, and initiated oviduct growth (to 31% of mature size). However, estradiol treatment caused no change in mass of pectoral muscle, heart or liver, demonstrating that there is no simple relationship between onset of reproductive development and associated tissue mass changes.     

Fine structural basis of the cutaneous water barrier in nestling Zebra Finches Poephila guttata

Transepidermal water loss was studied in nestlings, fledglings and adults of the xerophylic Zebra Finch Poephila guttata. Nestlings lose little water (2–4 ppm/0–5 cm²/h) through the skin as compared to adults (60–70 ppm/0–5 cm²/h). Light and electron microscopic examination of the skin sections of both age classes revealed an abundance of lipids in the form of vacuoles and large multigranular bodies in the epidermis of nestlings, but few such lipid bodies in the epidermis of adults. Some of the disc-like contents of granular bodies appear to be extruded into the intercellular spaces. Based on earlier studies with mammals and reptiles, it is concluded that epidermal lipids are the basis of the integumentary permeability barrier in nestlings.     

Ontogeny of Adaptive Antibody Response to a Model Antigen in Captive Altricial Zebra Finches

Based on studies from the poultry literature, all birds are hypothesized to require at least 4 weeks to develop circulating mature B-cell lineages that express functionally different immunoglobulin specificities. However, many altricial passerines fledge at adult size less than four weeks after the start of embryonic development, and therefore may experience a period of susceptibility during the nestling and post-fledging periods. We present the first study, to our knowledge, to detail the age-related changes in adaptive antibody response in an altricial passerine. Using repeated vaccinations with non-infectious keyhole limpet hemocyanin (KLH) antigen, we studied the ontogeny of specific adaptive immune response in altricial zebra finches Taeniopygia guttata. Nestling zebra finches were first injected at 7 days (7d), 14 days (14d), or 21 days post-hatch (21d) with KLH-adjuvant emulsions, and boosted 7 days later. Adults were vaccinated in the same manner. Induced KLH-specific IgY antibodies were measured using ELISA. Comparisons within age groups revealed no significant increase in KLH-specific antibody levels between vaccination and boost in 7d birds, yet significant increases between vaccination and boost were observed in 14d, 21d, and adult groups. There was no significant difference among age groups in KLH antibody response to priming vaccination, yet KLH antibody response post-boost significantly increased with age among groups. Post-boost antibody response in all nestling age groups was significantly lower than in adults, indicating that mature adult secondary antibody response level was not achieved in zebra finches prior to fledging (21 days post-hatch in zebra finches). Findings from this study contribute fundamental knowledge to the fields of developmental immunology and ecological immunology and strengthen the utility of zebra finches as a model organism for future studies of immune ontogeny.     

Sex Allocation in Response to Maternal Condition: Different Tactics of Care-Giving by Male and Female Zebra Finches

While behavioral ecologists have studied sex allocation for 30 yr, almost nothing is known about the roles of male vs. female parents in making secondary allocation decisions in species with bi‐parental care. To investigate possible sex differences in tactics in zebra finches, we manipulated the condition of one cohort of females by trimming their flight feathers; a second cohort of females and all males were left intact. Focal observations of feeding behavior revealed that manipulated females did not reduce their feeding time, but rather focused their efforts on rearing sons, while control females allocated effort to rearing daughters. Males mated to manipulated females tended to focus effort to daughters, while control males showed no consistent response. Manipulated females experienced a lower reproductive rate, primarily because of a low daughter rate, relative to control females. Manipulated females also laid smaller clutches and had longer inter‐clutch intervals, which suggest that their ability to metabolize and allocate essential proteins from pectoral muscle mass during the egg‐laying period was impaired. To our knowledge, this study is the first to show that parents of both sexes make active sex allocation decisions when the physiological condition of one parent is manipulated; males do not simply adopt female allocation patterns, but make complementary adjustments. Our results have implications for interpretation of handicapping studies that seek to understand the dynamics of inter‐sexual negotiations of care‐giving. Investigation of sex differences in sex allocation tactics in species with limited dietary protein, such as granivorous birds, is a potentially important direction for future research.     

Correlates and Consequences of Dominance in a Social Rodent

In harem‐polygynous societies, body condition is often correlated with dominance rank. However, the consequences of dominance are less clear. High‐ranking males do not inevitably have the highest reproductive success, especially in systems where females mate with multiple males. In such societies, we expect male reproductive success to be more highly skewed than female reproductive success, but reproductive skew in females can still arise from rankings established within matrilineal societies. Dominance can also impact life‐history decisions by influencing dispersal patterns in yearlings. To better understand the function of dominance in harem‐polygynous societies, we studied the causes and consequences of dominance in yellow‐bellied marmots (Marmota flaviventris), a social rodent with skewed male reproductive success and female reproductive suppression. Specifically, we examined body condition as a predictor and the probability of breeding, number of offspring, and dispersal as outcomes of dominance. Additionally, we looked at variation in dominance between males and females and adults and yearlings, because marmots can engage in distinct interactions depending on the type of individuals involved. We found that marmots in better body condition have higher dominance rank than those in poorer condition. In addition, adults are dominant over yearlings. Within yearlings, dominance does not influence dispersal, but those in better body condition are less likely to disperse. Within all adults, individuals in better condition produce more offspring per year. Within adult males, more dominant males have greater reproductive success. Despite previous evidence of reproductive suppression in females, we found no effects of dominance rank on female reproductive success in the current study. The function of dominance in female marmots remains enigmatic.