Sex differences in the telencephalic song control circuitry in Bengalese finches (Lonchura striata var. domestica)

Bengalese finches, Lonchura striata, are extremely sexually dimorphic in their singing behavior; males sing complex songs, whereas females do not sing at all. This study describes the developmental differentiation of the brain song system in Bengalese finches. Nissl staining was used to measure the volumes of four telencephalic song nuclei: Area X, HVC, the robust nucleus of the arcopallium (RA), and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN). In juveniles (circa 35 days old), Area X and the HVC were well developed in males, while they were absent or not discernable in females. The RA was much larger in males but barely discernable in females. In males, the volumes of Area X and the RA increased further into adulthood, but that of the HVC remained unchanged. The LMAN volume was greater in juveniles than in adults, and there was no difference in the LMAN volume between the sexes. The overall tendency was similar to that described in zebra finches, except for the volume of the RA, where the degree of sexual dimorphism is larger and the timing of differentiation occurs earlier in Bengalese finches. Motor learning of the song continues until day 90 in zebra finches, but up to day 120 in Bengalese finches. Earlier neural differentiation and a longer learning period in Bengalese finches compared with zebra finches may be related to the more elaborate song structures of Bengalese finches.     

Syringeal specialization of frequency control during song production in the Bengalese finch (Lonchura striata domestica)

Background

Singing in songbirds is a complex, learned behavior which shares many parallels with human speech. The avian vocal organ (syrinx) has two potential sound sources, and each sound generator is under unilateral, ipsilateral neural control. Different songbird species vary in their use of bilateral or unilateral phonation (lateralized sound production) and rapid switching between left and right sound generation (interhemispheric switching of motor control). Bengalese finches (Lonchura striata domestica) have received considerable attention, because they rapidly modify their song in response to manipulations of auditory feedback. However, how the left and right sides of the syrinx contribute to acoustic control of song has not been studied.

Methodology

Three manipulations of lateralized syringeal control of sound production were conducted. First, unilateral syringeal muscular control was eliminated by resection of the left or right tracheosyringeal portion of the hypoglossal nerve, which provides neuromuscular innervation of the syrinx. Spectral and temporal features of song were compared before and after lateralized nerve injury. In a second experiment, either the left or right sound source was devoiced to confirm the role of each sound generator in the control of acoustic phonology. Third, air pressure was recorded before and after unilateral denervation to enable quantification of acoustic change within individual syllables following lateralized nerve resection.

Significance

These experiments demonstrate that the left sound source produces louder, higher frequency, lower entropy sounds, and the right sound generator produces lower amplitude, lower frequency, higher entropy sounds. The bilateral division of labor is complex and the frequency specialization is the opposite pattern observed in most songbirds. Further, there is evidence for rapid interhemispheric switching during song production. Lateralized control of song production in Bengalese finches may enhance acoustic complexity of song and facilitate the rapid modification of sound production following manipulations of auditory feedback.     

Genetic and developmental effects, and morphological influences on the acoustic structure of individual distance calls in female Bengalese finches Lonchura striata var. domestica

Recent studies of the vocal mechanisms of songbirds have shown that there are physical effects on sound production. Interspecific and phylogenetic comparisons have shown that body mass and bill morphology are two major factors affecting vocalizations such as songs. We analyzed the distance calls of female Bengalese finches Lonchura striata var. domestica , the non-vocal learning sex, to assess the potential physical effects on the acoustic structure of vocalizations. By experimentally controlling rearing condition using cross-fostering we could examine the effects of the developmental environment and genetic background. None of the tested factors affected the peak frequency of the distance calls, but we found that larger-billed birds tended to produce shorter bout calls with higher trill rates. These results suggest that the divergence of bill morphology can affect acoustic features at the within-population level. We also found that the birds reared in the same foster brood and siblings from the same genetic parents tended to produce calls with similar trill rates. This implies that the trill rate is under the influence of developmental and genetic factors.     

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

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

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。     

Uropygial gland volatiles may code for olfactory information about sex,individual, and species in Bengalese finches Lonchura striata

Over-shadowed by eye-catching vocal and visual signals, chemical communication has long been overlooked in birds. This study aimed at exploring whether volatile composition of the uropygial gland secretion （UGS） of birds was associated with the information about sex, individual and species. By using dichloromethane extraction and gas chromatography-mass spectrometry （GC-MS）, we analyzed the UGS volatiles of domesticated Bengalese finches （ Lonchura striata, Estrildiea） which is also known as white-rumped munias. We characterized 16 volatile molecules from the UGS, including eight n-alkanols, five diesters, an ester, an aldehyde and a fatty acid, and quantified them in terms of GC peak area percentages （relative abundances） . Among these compounds, hexadecanol and octadecanol were major components in both sexes. The former was richer in males than in females and the latter richer in females than in males, suggesting that they might be male and female pheromone candidates, respectively. The high inter-individual variations, in relative abundance, of the UGS volatiles implied that these compounds might carry information about individuality. The similarity between GC profiles of the UGS and wing feather from same individuals indicates that the birds might preen the secretion to their feathers to transmit chemical cues. Additionally, by comparing with three sympatric passerine species, i. e., zebra finches Taeniopygia guttata, yellow-bowed buntings Emberiza chrysophrys and rooks Corvus frugilegus, we found that the composition of C13 - C18 alkanols in the UGS might code for information about species. Our study also showed that quantitative differences （degree） of same UGS volatiles might be the key for the Bengalese finch to code for information about sex and individuality whereas both the kind and degree of UGS constituents could be utilized to code for information about species [ Current Zoology 55 （5）： 357-365, 2009].     

Uropygial gland volatiles may code for olfactory information about sex,individual,and species in Bengalese finches Lonchura striata

Over-shadowed by eye-catching vocal and visual signals,chemical communication has long been overlooked in birds.This study aimed at exploring whether volatile composition of the uropygial gland secretion(UGS)of birds was associated with the information about sex,individual and species.By using dichloromethane extraction and gas chromatography-mass spectrometry(GC-MS),we analyzed the UGS volatiles of domesticated Bengalese finches(Lonchura striata,Estrildiea)which is also known as white-rumped munias.We char...     

Vorbildwahl in der Gesangsentwicklung beim Japanischen Mövchen (Loncbura striata var. domestica,Estrildidae)

Birds which must learn their species-specific song need a means for choosing the appropriate song model. As individual Bengalese Finch ♂♂ have distinctive songs and song elements it is possible to determine a juvenile's choice of song models from within a restricted population. The results suggest that after an early period of learning from several models, juveniles preferentially copy the song of their father.     

Song Learning in Wild and Domesticated Strains of White‐Rumped Munia,Lonchura striata,Compared by Cross‐Fostering Procedures: Domestication Increases Song Variability by Decreasing Strain‐Specific Bias

Song diversity results from the interactions between natural selection, sexual selection, and individual learning. To understand song diversity, all three factors must be considered collectively, not separately. Bengalese Finches were domesticated about 250 yr ago. Their courtship songs have become different from their ancestor, the White‐rumped Munia. Bengalese Finches sing songs with complex note‐to‐note transition patterns and with acoustically diverse song notes while White‐rumped Munias sing songs with fixed note sequence and mostly broad band song notes. Bengalese Finches were selected for domestication based on their good parenting ability, not their songs, but this artificial selection has nonetheless affected their songs. To test whether divergence occurred not only in the song phenotypes but also in the genetic basis for predisposition of strain specific song learning, we conducted a cross‐fostering experiment between Bengalese Finches and White‐rumped Munias. In both strains, song learning was affected by rearing condition: the acoustical feature and transition patterns followed those of the foster fathers. However, the accuracy of song learning differed between the wild and the domesticated strains: sharing of song note between sons and tutors in Finches was not very accurate regardless of the tutor, while Munias were highly accurate in copying Munia songs but often omitted song elements from Finch fathers. These results suggest that White‐rumped Munias are strongly constrained to learn their own strain’s song, and that this constraint was relaxed in the Bengalese Finch by domestication.     

Cognitive tactics of Bengalese finch (<Emphasis Type="Italic">Lonchura striata </Emphasis>var. <Emphasis Type="Italic">domestica</Emphasis>) for song discrimination in a go/no-go operant task

Twelve Bengalese finches (Lonchura striata var. domestica) were trained to discriminate between a conspecific and a heterospecific song in a go/no-go operant task. Training the birds to go for the conspecifics song or to go for the heterospecific song required the same number of training sessions. Nine possible cognitive tactics could be used to solve this task, but probe tests revealed that the birds used only four. Six birds memorized only the “no-go” stimulus and responded to the rest of the stimuli (no-go memory), two birds classified songs according to the species category (open-ended categorization), one bird memorized both of the training stimuli but responded by chance to the probe stimuli (rote categorization), and two birds combined open-ended and rote categorization tactics (combined categorization). These tactics were related to the number of sessions needed to reach the species-discrimination criterion. Our results suggest that investigators should consider individual cognitive tactics and the pitfalls of go/no-go discrimination when interpreting the results of operant discrimination tasks.     

Song Motor control organizes acoustic patterns on two levels in Bengalese finches (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

Based on statistical analyses of song sequences, Bengalese finch (Lonchura striata var. domestica) songs do not show unvarying motif repetition as has been found in zebra finches (Taeniopygia guttata). Instead, there are variations of partially stereotyped sequences of song syllables. Although these stereotyped sequences consist of multiple syllables, in most cases these syllables occur together. To examine whether such structures really exist as a vocal production unit, we subjected singing birds to a light flash and determined when the stimulus stopped the songs. When light interruptions were presented within the statistically stereotyped sequences, the subsequent syllables tended to be produced, whereas interruptions presented during the statistically variable sequences tended to cause instantaneous song termination. This suggests that the associations among the song syllables that compose the statistically stereotyped sequences are more order dependent than those for the statistically variable sequences, and the tolerances of syllable pairs to visual interruptions are consistent with the statistical song structures. Additionally, following interruptions, several types of song sequence variations were observed that had not been previously reported. These phenomena might be caused by various effects of the visual stimulus on the hierarchical motor control program.     

Cues for Early Discrimination of Conspecific Song in the White-Crowned Sparrow (Zonotrichia leucophrys)

In song learning, white-crowned sparrows ( Zonotrichia leucophrys ) begin memorizing conspecific song models at around 20 d of age. Even prior to song memorization, however, between 10 and 20 d of age, these birds respond differently to playbacks of conspecific and heterospecific songs. To investigate the acoustic cues underlying this early song discrimination, we measured the vocal responses of newly fledged young to playbacks of modified conspecific and heterospecific songs. Fledgling white-crowned sparrows responded more strongly to songs containing conspecific notes than to songs containing notes from other species. In contrast, the presence or placement of an introductory whistle, present in all white-crowned sparrow songs, did not affect response levels. A whistle has previously been shown to serve as an acoustic cue for song memorization and production in this species. Such different responses to the species-typical introductory whistle at different stages suggests that developmental changes occur in the template system underlying song learning, the factors governing song recognition, or both.     

A new PCR-RFLP within the domestic pigeon (Columba livia var. domestica) cytochrome b (MTCYB) gene

A total of 244 domestic pigeons (Columba livia var. domestica) were genotyped using the PCR-RFLP method. A 999 bp fragment of the MTCYB gene was amplified. The amplification products were digested with restriction enzymes. PCR-RFLP for MvaI restriction enzyme was observed. Frequencies of alleles were as follows: MTCYB(C)--0.926, MTCYB(G)-- 0.074. The frequencies of MTCYB/MvaI alleles found in this study for non-homing pigeons considerably deviate from the values found for homing/racing pigeons (allele MTCYB(G) occurred only in the non-homing breeds).     

PCR-RFLPs within the lactate dehydrogenase (LDH-A) gene of the domestic pigeon (Columba livia var. domestica)

A total of 45 racing pigeons were genotyped using PCR-RFLP method. PCR product of the LDH-A gene was amplified according to the Long-PCR procedure. The amplification products were digested with restriction enzymes. PCR-RFLPs for two restriction enzymes, HaeIII and NlaIV, were observed. Two pairs of alleles LDH-A(A) and LDH-A(B) for LDH-A-NlaIV polymorphism and LDH-A(C) and LDH-A(D) for LDH-A-HaeIII polymorphism were detected in the homozygous and heterozygous states. Frequencies of alleles were as follows: A - 0.622, B - 0.378 and C - 0.256, D - 0.744.     

The effect of sound location in a song-discrimination task by Bengalese finches (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

To understand the relationship between song perception and stimulus location, Bengalese finches were trained to discriminate between a normally played conspecific song and the reversed song. Loudspeakers on the opposite side of the response key (experimental condition) and above the subject (control condition) were used to present stimuli. All control birds learned the task, whereas some experimental subjects did not. In general, controls learned the task more quickly than experimental animals. These results suggest that sound location may be closely associated with behavioral responses in this species. Bioacoustical investigations should be performed while taking these results into consideration.     

Role of VA-mycorrhiza in growth and mineral nutrition of apple (Malus pumila var.domestica) rootstock cuttings

One-year-old apple cuttings (Malus pumila var.domestica cv. M26) were grown for 6 months in pot culture with and without inoculum of the VA-mycorrhizal fungus (VAMF)Glomus macrocarpum in soil from a long-term fertilizer field experiment with different P availability (20, 210, and 280 mg CAL-extractable P kg⁻¹). The indigenous VAMF propagule density was reduced by 0.5 Mrad X-irradiation. At harvest, non-inoculated and inoculated plants had similar proportions of root length bearing vesicles. Net dry weight of tree cuttings was significantly increased by inoculation only at 20 mg P kg⁻¹ (+62%). Increasing P availability from 210 to 280 mg P kg⁻¹ led to a 4-week depression of shoot elongation rate only in the inoculated plants. Uptake of P was significantly enhanced by inoculation at 20 and 210 mg P kg⁻¹ (+64 and +12%, respectively). On average, inoculated plants had significantly higher concentrations of Zn in leaves and in roots (+16 and +14%, respectively) and of copper in stems and in roots (+13 and +126%, respectively). Proportion of vesicle bearing root length was significantly correlated with root caloric content. A lipid content of 0.9–4.5% in the root dry matter was attributed to the presence of vesicles corresponding to 1.6–8.2% of total root caloric content. As the control plants were also infected, the beneficial effect of VA-mycorrhiza on nutrient uptake and growth of apple cuttings was underestimated at all P levels. Furthermore, VAM-potential at the lowest P level was not fully exploited as onset of infection was most certainly delayed because of a decreased photosynthetic rate due to P deficiency. Energy drain by VAMF-infection was most probably underestimated considerably, due to, among others, loss of infected root cortex during root growth, sampling and staining. It is concluded that apple cuttings rely on VA-mycorrhizal P-uptake at least in low P soils. In high P soils, apple cuttings may profit predominantly from the uptake of Zn and Cu by the fungal symbionts.     

Apple (Malus pumila var. domestica) phenology is advancing due to rising air temperature in northern Japan

Recent studies show advancing onset of plant growing season in many regions for the last several decades. With the well‐established dependence of plant phenology on temperature, these trends are interpreted as an indication of global warming. For several decades, however, other determinants of plant phenology, e.g. varieties and trends in managed systems, may have changed and confounded the phenological trends. In this study, we tested if long‐term changes in phenology of apple (Malus pumila var. domestica) are attributable to long‐term changes in temperature by comparing the phenological response to long‐term trend in air temperature, which is of our interest, with that to year‐to‐year fluctuation in air temperature, which should represent the real effect of temperature on phenology. We collected records of air temperature and phenological events (budding and flowering) in apple from 1977 to 2004 at six locations in Japan. Linear trends in flowering showed advancing rate in the range from 0.21 to 0.35 day yr^?1, statistically significant at three locations (P<0.05). We also found a warming trend in mean air temperature throughout March and April, with which flowering was closely correlated, in the range from 0.047 to 0.077 °C yr^?1, statistically significant at five locations (P<0.05). We separated the temperature time‐series into two components: a long‐term trend and a year‐to‐year fluctuation, by fitting smoothing spline to the trend and taking the residuals as the anomaly. We then fit a multiple regression model of phenological response to air temperature with separate coefficients for long‐term trend and anomaly. Flowering date responded to the long‐term trend at ?3.8 day °C^?1 and to the anomaly at ?4.6 day °C^?1. The temperature coefficients were not statistically different from each other or among locations, suggesting that the advance of apple phenology has predominantly been caused by the temperature increase across the locations studied. The same result was also observed with budding.