Electromyographic studies of the syrinx in parrots (Aves,Psittacidae)

Summary The vocal organ (syrinx) of a bird may contain either extrinsic muscles alone or both extrinsic and intrinsic muscles. The former arise and insert on the trachea and affect the syrinx only indirectly; the latter also arise on the trachea but insert directly on syringeal elements. It is widely supposed that syringeal muscles can affect modulations of the sounds the birds make, and further, that the intrinsic muscles are closely associated with such a function. However, the exact roles of the two groups of muscles have not been directly observed.The psittacid syrinx, which has one (for practical purposes) pair of extrinsic and two pairs of intrinsic muscles, is about as simple as one can find in birds capable of uttering a wide variety of sounds. We have taken electromyograms from the syringeal muscles of five species of parrots. In all of these, the extrinsic sternotrachealis showed the simple activation pattern activity previously described from several non-passerine species that possess only extrinsic muscles. The intrinsic muscles, however, showed a variety of activity patterns. The relatively simple call of Cyanoliseus patagonus again showed the simple activation pattern. In Myiopsitta monachus, the muscles showed a string of pulses that matched to pulses of sound in a strongly amplitude modulated call. Agapornis roseicollis used at least two distinct patterns, each associated with a different call.The results are consistent with an hypothesis that, because of their indirect attachment of the syrinx, extrinsic muscles are poorly suited to the production of precise, rapid changes in syringeal action, but rather will function in an on-off switch capacity. Intrinsic muscles are so situated that, given proper neurological stimulus, they can effect a variety of alterations in the sound pattern. Hence, intrinsic muscles are necessary for the evolution of large vocabularies and variable vocal behavior.     

Sexual Dimorphism of the Zebra Finch Syrinx Indicates Adaptation for High Fundamental Frequencies in Males

Background

In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior.

Methodology/Principal Findings

Here we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency.

Conclusions/Significance

The syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.     

Mechanisms of song production in the Australian magpie

Australian magpies (Gymnorhina tibicen) are notable for their vocal prowess. We investigated the syringeal and respiratory dynamics of vocalization by two 6-month-old males, whose songs had a number of adult features. There was no strong lateral syringeal dominance and unilateral phonation was most often achieved by closing the syringeal valve on the contralateral side of the syrinx. Unlike other songbirds studied, magpies sometimes used an alternative syringeal motor pattern during unilateral phonation in which both sides of the syrinx are partially adducted and open to airflow. Also, in contrast to most other songbirds, the higher fundamental frequency during two-voice syllables was usually generated on the left side of the syrinx. Amplitude modulation, a prominent feature of magpie song, was produced by linear or nonlinear interactions between different frequencies which may originate either on opposite sides of the syrinx or on the same side. Pulse tones, similar to vocal fry in human speech, were present in some calls. Unlike small songbirds, the fundamental of the modal frequency can be as low as that of the pulse tone, suggesting that large birds may have evolved pulse tones to increase acoustic diversity, rather than decrease the fundamental frequency.     

Penguins use the two-voice system to recognize each other

The sound-producing structure in birds is the syrinx, which is usually a two-part organ located at the junction of the bronchi. As each branch of the syrinx produces sound independently, many birds have two acoustic sources. Thirty years ago, we had anatomical, physiological and acoustical evidence of this two-voice phenomenon but no function was known. In songbirds, often these two voices with their respective harmonics are not activated simultaneously but they are obvious in large penguins and generate a beat pattern which varies between individuals. The emperor penguin breeds during the Antarctic winter, incubating and carrying its egg on its feet. Without the topographical cue of a nest, birds identify each other only by vocal means when switching duties during incubation or chick rearing. To test whether the two-voice system contains the identity code, we played back the modified call of their mate to both adults and also the modified call of their parents to chicks. Both the adults and the chicks replied to controls (two voices) but not to modified signals (one voice being experimentally suppressed). Our experiments demonstrate that the beat generated by the interaction of these two fundamental frequencies conveys information about individual identity and also propagates well through obstacles, being robust to sound degradation through the medium of bodies in a penguin colony. The two-voice structure is also clear in the call of other birds such as the king penguin, another non-nesting species, but not in the 14 other nesting penguins. We concluded that the two-voice phenomenon functions as an individual recognition system in species using few if any landmarks to meet. In penguins, this coding process, increasing the call complexity and resisting sound degradation, has evolved in parallel with the loss of territoriality.     

Lateralization of syringeal function during song production in the canary

The canary (Serinus canaria) vocal organ, the syrinx, has two separate sound sources, one in the cranial end of each bronchus. Previous investigations of whether song syllables are produced unilaterally or bilaterally have provided two contradictory results, as one researcher suggested that almost all syllables are produced by the left side of the syrinx alone, whereas another researcher suggested that both sides contribute similarly to all syllables. Our experiments, which involved unilateral bronchus plugging followed later by denervation of the ipsilateral syringeal muscles, attempted to resolve this disagreement. The males with right bronchus plugs, singing on the left side of the syrinx alone, produced nearly normal songs, whereas the birds with left bronchus plugs, singing on the right side, sang quite poorly. Interpretation of these data is difficult because it is not clear how syringeal function would be affected if the airflow rate through the intact side is increased above normal, nor is it known if the bird can compensate for bronchus occlusion. Nonetheless, we suggest that in male canaries most syllables are normally sung by the left side alone, with some syllables being produced by the right side alone and some being sung by both sides together. Right nerve section had little effect on the right-bronchus-plugged males' ability to sing, but the repertoires of the left-plugged males were altered after left nerve section, indicating the possibility that signals carried by the left nerve exert an influence on the contralateral side.     

Bilateral song production in domestic canaries

We studied the mechanism of song production in the outbred common or domestic canary (Serinus canaria). The contribution that each side of the syrinx makes to song was investigated by observing the effect of unilaterally occluding the left or right primary bronchus, followed by section of the ipsilateral branch of the tracheosyringeal nerve. In other birds with a bilaterally intact vocal system we monitored airflow through each side of the syrinx, together with subsyringeal pressure, during spontaneous song. Song production by domestic canaries is not strongly lateralized as it is in the conspecific song-bred waterslager strain. Some syllables are produced entirely on the left or right side of the syrinx, whereas others contain sequential contributions from each side. Low fundamental frequencies are produced with the left syrinx and high frequencies by the right syrinx, increasing the frequency range of domestic canary song compared to that of the waterslager strain. Midrange frequencies can be generated by either side. Syllables at repetition rates below about 25 s(-1) were accompanied by minibreaths, which were usually bilateral. Unilateral minibreaths were typically on the left side. At higher syllable repetition rates, minibreaths were replaced by a respiratory pattern of pulsatile expiration. Our data show that strong unilateral dominance in song production, present in the waterslager strain, is not a trait of the species as a whole and that the pattern of song lateralization can be altered by selective breeding for particular song characteristics.     

Phonation in the Orange-winged Amazon parrot,Amazona amazonica

Summary The syrinx of the Orange-winged Amazon parrot includes two external tympaniform membranes thought to be involved in sound production. The position of these membranes at the confluence of the bronchial and tracheal lumina requires that during phonation they be driven by a single column of air and by its attending turbulence patterns. Because of this anatomical arrangement, the phonatory output of either right or left syringeal half is grossly affected by denervation of the ipsilateral or contralateral syringial muscles. Following unilateral syringeal denervation the unbalanced oscillation of the two external tympaniform membranes generates noise. Form this we may infer that normally the parrot syrinx acts as a unitary sound source. Syringeal innervation is provided by the tracheosyringealis branch of the hypoglossus nerve. Each tracheosyringealis innervates both syringeal halves. Section of either the right or left tracheosyringealis leads to a minor and temporary change in the structure of vocalization. One week after the operation the vocalizations are delivered as pre-operatively. There is no indication of either right or left hypoglossal dominance in the phonatory control of the parrot syrinx. Other observations presented here are used to speculate on the possible role of the parrot tongue in altering the resonating properties of the nasopharyngeal space and generating speech like formants.     

Motor dynamics of song production by mimic thrushes

In brown thrashers (Toxostoma rufum) and grey catbirds (Dumetella carolinensis) neither side of the syrinx has a consistently dominant role in song production. During song, the two sides operate independently, but in close cooperation with each other and with the respiratory muscles which are capable of adjusting expiratory effort to maintain a constant rate of syringeal airflow despite sudden changes in syringeal resistance. Phonation is frequently switched from one side of the syrinx to the other, both between syllables and within a syllable. When both sides of the syrinx produce sound simultaneously, their respective contributions are seldom harmonically related. The resulting “two-voice” syllables sometimes contain difference tones with prominent sinusoidal amplitude modulation (AM). Rarely, both sides simultaneously produce the same sound. In general, however, the frequency range of sound contributed by the right syrinx is higher than that of the left syrinx. The right syrinx is also primarily responsible for producing a rapid cyclical amplitude modulation which is a characteristic feature of some syllables. This kind of AM is generated by either repetitive brief bursts of sound from the right side that modulate the amplitude of a continuous sound arising on the left side or cyclically opening the right syrinx, allowing unmodulated expiratory air to bypass the phonating left side. 1994 John Wiley & Sons, Inc.     

Left hypoglossal dominance in the control of canary and white-crowned sparrow song

Summary The syrinx of songbirds includes two separate sound sources, the internal tympaniform membranes (ITM), which form the medial wall of each bronchus. The performance of each ITM is controlled by the muscles of that syringeal half. In the canarySerinus canarius, hypoglossal fibers reaching the syrinx via the tracheosyringealis branch of the hypoglossus are responsible for sound modulation. The muscles controlling the performance of the left syringeal half are innervated solely by the left tracheosyringealis; those controlling the right syringeal half are innervated only by the right tracheosyringealis. In the canary and white-crowned sparrow (Zonotrichia leucophrys) a great majority of song elements disappears after section of the left tracheosyringealis, yet remains intact after section of the right one. This phenomenon, earlier described in the chaffinch (Nottebohm, 1970, 1971, 1972) and confirmed in the white-throated sparrow (Lemon, 1973), has been called left hypoglossal dominance. Left hypoglossal dominance occurs in canaries with small or large song repertoires. It occurs in chronically deafened canaries that never had access to their own auditory feedback; it also occurs in birds that had the right or left cochlea removed at an early age. To this extent, left hypoglossal dominance seems to emerge in the individual as a motor phenomenon.We wish to thank Betsy Manning for all the time and effort she spent recording the song of our birds. We are also indebted to Professor Peter Marler, Rockefeller University, for letting us include in our study several birds which he reared in noise and which formed part of an earlier experiment (Marler et al., 1973). Our research was supported by NIH grant MH 18343.     

Functional morphology of the tongue muscles of some Indian insect-eating birds

In the complex feeding apparatus of birds, the tongue muscles also play an important role like the jaw muscles. Among the passerine birds, the tongue muscles exhibit greater structural uniformity than the jaw muscles. The elaborate system of extrinsic tongue musculature brings about all necessary movements of the tongue. The intrinsic tongue musculature in all the birds studied is extremely weak and reduced. The principal tongue muscles are better developed in Turdoides and Copsychus than in the other birds. However, in Orthotomus, Anthus, Dicrurus, and Merops, some of the tongue muscles are quite well developed, perhaps compensating for the deficiencies of the other muscles. The origin of M. branchiomandibularis posterior from the outer mandibular ramus in Orthotomus, Dicrurus, and Merops is remarkable, but its occurrence may not be unusual among the passerine birds. Some variations are also observed in the origin and insertion of M. genioglossus in Turdoides, Copsychus, and Anthus. The correlations between the structures and functions of the tongue muscles are not always possible without considering the synergistic actions of the other muscles.     

Motor mechanisms of a vocal mimic: implications for birdsong production

The diverse vocal performances of oscine songbirds are produced by the independent but coordinated patterns of activity in muscles controlling separate sound generators on the left and right sides of their duplex vocal organ, the syrinx. Species with different song styles use the two sides of their syrinx in different ways to produce their species-typical songs. Understanding how a vocal mimic copies another species' song may provide an insight into whether there are alternative motor mechanisms for generating the model's song and what parts of his song are most difficult to produce. We show here that when a vocal mimic, the northern mockingbird, accurately copies the song of another species it also uses the vocal motor pattern employed by the model species. Deviations from the model's production mechanism result in predictable differences in the mockingbird's song. Species-specific acoustic features of the model seem most difficult to copy, suggesting that they have been exposed to the strongest selective pressure to maximize their performance.     

Superfast vocal muscles control song production in songbirds

Birdsong is a widely used model for vocal learning and human speech, which exhibits high temporal and acoustic diversity. Rapid acoustic modulations are thought to arise from the vocal organ, the syrinx, by passive interactions between the two independent sound generators or intrinsic nonlinear dynamics of sound generating structures. Additionally, direct neuromuscular control could produce such rapid and precisely timed acoustic features if syringeal muscles exhibit rare superfast muscle contractile kinetics. However, no direct evidence exists that avian vocal muscles can produce modulations at such high rates. Here, we show that 1) syringeal muscles are active in phase with sound modulations during song over 200 Hz, 2) direct stimulation of the muscles in situ produces sound modulations at the frequency observed during singing, and that 3) syringeal muscles produce mechanical work at the required frequencies and up to 250 Hz in vitro. The twitch kinematics of these so-called superfast muscles are the fastest measured in any vertebrate muscle. Superfast vocal muscles enable birds to directly control the generation of many observed rapid acoustic changes and to actuate the millisecond precision of neural activity into precise temporal vocal control. Furthermore, birds now join the list of vertebrate classes in which superfast muscle kinetics evolved independently for acoustic communication.     

Contributions of syringeal muscles to respiration and vocalization in the zebra finch

Acute and chronic electromyographic (EMG) recordings from individual syringeal muscles were used to study syringeal participation in respiration and vocalization. In anesthetized birds, all syringeal muscles recorded were active to some degree during the expiratory phase of respiration, following activity in the abdominal musculature and preceding the emergence of breath from the nostril. In awake birds, the ventralis (V) muscle fired a strong, consistent burst, but the dorsalis (D) was variable both in strength and timing. Denervation of V is sufficient to produce the wheezing respiration originally seen in birds with complete bilateral section of the tracheosyringeal nerve. Complete syringeal denervation also removed almost all the acoustic features that distinguish individual song syllables, but had a minor effect on the temporal structure of song. When activity in V and D was recorded in awake, vocalizing birds, D was active before and during sound production, and V showed a small burst before sound onset and a vigorous burst timed to the termination of sound. During song, V was consistently active at sound offset, but also participated during sound for narrow bandwidth syllables. For some syllables (simple harmonic stacks), neither muscle was active. These data suggest that V contributes to syllable termination during vocalization and may silence the syrinx during normal respiration. D contributes to the acoustic structure of most syllables, and V may contribute to a special subset of syllables. In summary, the syringeal muscles show different activity patterns during respiration and vocalization and can be independently activated during vocalization, depending on the syllable produced.     

Molecular Forms of Acetylcholinesterase: Regulation in a Testosterone-Sensitive Nerve-Muscle Axis

We measured the distribution of molecular forms of acetylcholinesterase (AChE) in muscles of a song bird, the zebra finch, and found a pattern similar to those reported in other vertebrates. As in other species, the most rapidly sedimenting form of the enzyme decreases to barely detectable levels following denervation. In the muscles of the syrinx, castration causes a large decrease in AChE activity, but has little or no effect on the relative abundance of AChE forms. This suggests that the number of AChE catalytic sites is changing without affecting the distribution of catalytic sites among the molecular forms. This is in marked contrast with the effect of denervation in the syrinx, which causes changes in the distribution of activity, as well as in total activity.     

Peripheral control and lateralization of birdsong

Recent studies on several species of oscine songbirds show that they achieve their varied vocal performances through coordinated activity of respiratory, syringeal, and other vocal tract muscles in ways that take maximum advantage of the acoustic flexibility made possible by the presence of two independently controlled sound sources in their bipartite syrinx (vocal organ). During song, special motor programs to respiratory muscles alter the pattern of ventilation to maintain the supply of respiratory air and oxygen to permit songs of long duration, high syllable repetition rates, or maximum spectral complexity. Each side of the syrinx receives its own motor program that, together with that sent to respiratory muscles, determines the acoustic properties of the ipsilaterally produced sound. The acoustic expression of these bilaterally distinct, phonetic motor patterns depends on the action of dorsal syringeal adductor muscles that, by opening or closing the ipsilateral side of the syrinx to airflow, determine the amount each side contributes to song. The syringeally generated sound is further modified by muscles that control the shape of the vocal tract. Different species have adopted different motor strategies that use the left and right sides of the syrinx in patterns of unilateral, bilateral, alternating, or sequential phonation to achieve the differing temporal and spectral characteristics of their songs. As a result, the degree of song lateralization probably varies between species to form a continuum from unilateral dominance to bilateral equality. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 632–652, 1997     

The anatomy of the syrinx in passerine birds

The macroscopical structure of the organ of voice in songbirds has long been known, but detailed information on the microscopical anatomy of the syrinx has generally been lacking. Observations based largely on macroscopical evidence have led to a number of erroneous interpretations of function of various syringeal components, and lacking microscopical information, the vocal mechanism of birds cannot be adequately understood.
A wide variety of passeriform bird syrinxes have been studied by means of serial sections. Although there is much less variation in syringeal anatomy amongst songbirds than there is in the other orders of birds, and although all songbird syrinxes conform to the same basic pattern, there is nevertheless marked variation in various syringeal components between different passerine groups. Variations in syringeal structure within families Corvidae ( Corvus corone, C. frugilegus ), Sturnidae ( Sturnus vulgaris, Gracula religiosa ), Turdidae ( Turdus merula, Erithacus rubecula ), Hirundinidae ( Delichon urbica ), Ploceidae ( Passer domesticus ) and Paridae ( Parus major, Aegithalos caudatus ) are described and discussed. The significance of these findings in relation to bird sound production is discussed.     

二滩水电站建成前后库区流域鸟类多样性初步研究

对二滩水库库区的鸟类进行野外调查,发现在水库建成前后的鸟类都是187种,但其种类组成不同,相同种类129种,占观察到的种类的68．98％,同时 发现四川省鸟类新纪录12种,对建成前后的鸟类相对数量和多样性进行对比分析后,发现在水库建成后,云南松林区,常绿阔叶林区和针阔叶混交林区3种生境的鸟为相对数量和物种多样性较建成前增高,均匀度变化不明显,农田耕作区的鸟类物种多样性和均匀度都降低;水库建成后,整个系统的鸟类β多样性略有下降,水域与其它生境的鸟类相似性很低,建成后农田耕作区与其它生境间的鸟类相似性比建成前有所降低,云南松林与另两种森林生境间的鸟类相似性变化不大,常绿阔叶林区和针阔叶混交林区的鸟类相似性增高,导致鸟类多样性变化的一个原因是生境复杂性降低。     

Functional morphology of the cranio‐mandibular complex of the Guira cuckoo (Aves)

The cranio‐mandibular complex is an important structure involved in food capture and processing. Its morphology is related to the nature of the food item. Jaw muscles enable the motion of this complex and their study is essential for functional and evolutionary analysis. The present study compares available behavioral and dietary data obtained from the literature with novel results from functional morphological analyses of the cranio‐mandibular complex of the Guira cuckoo (Guira guira) to understand its relationship with the zoophagous trophic habit of this species. The bite force was estimated based on muscle dissections, measurements of the physiological cross‐sectional area, and biomechanical modeling of the skull. The results were compared with the available functional morphological data for other birds. The standardized bite force of G. guira is higher than predicted for exclusively zoophagous birds, but lower than for granivorous and/or omnivorous birds. Guira guira possesses the generalized jaw muscular system of neognathous birds, but some features can be related to its trophic habit. The external adductor muscles act mainly during food item processing and multiple aspects of this muscle group are interpreted to increase bite force, that is, their high values of muscle mass, their mechanical advantage (MA), and their perpendicular orientation when the beak is closed. The m. depressor mandibulae and the m. pterygoideus dorsalis et ventralis are interpreted to prioritize speed of action (low MA values), being most important during prey capture. The supposed ecological significance of these traits is the potential to widen the range of prey size that can be processed and the possibility of rapidly capturing agile prey through changes in the leverage of the muscles involved in opening and closing of the bill. This contributes to the trophic versatility of the species and its ability to thrive in different habitats, including urban areas.     

Non-random distribution of ring recoveries from trans-Saharan migrants indicates species-specific stopover areas

Many long-distance migrant birds regularly have to pass ecological barriers, like the Saharan desert, where fuelling is very difficult, and large fuel loads have to be stored in advance. In this paper, we have investigated how seven species of birds are distributed in autumn close to the Saharan desert in the eastern Mediterranean area by using ring recoveries from northern Europe. The result clearly shows that the species included are not randomly distributed at this point, about 3,000 km from the breeding area. Birds from rather large breeding areas were shown to converge in confined areas, which in several cases completely differ between species. This means that birds of the same species have to follow different migratory directions depending on the location of their starting point. The observed pattern support earlier findings indicating that birds, in combination with a clock-and-compass orientation procedure, must use some external cues in order to find confined species-specific areas. The possibility for birds to use information from the Earth's magnetic field as an external cue in this area is discussed.     

Moult strategies of Cory’s Shearwaters Calonectris diomedea borealis: the influence of colony location, sex and individual breeding status

The replacement of old feathers is essential for birds, but it is also an energy-demanding task. As moult usually does not coincide with other stressful events in its annual cycle, such as reproduction and migration, the bird can optimise its use of time and energy allocated to different activities. There are very few studies comparing the moult strategies of populations with similar breeding calendars but occurring in areas of different habitat quality. Cory’s Shearwaters Calonectris diomedea have a partial moult–breeding overlap, an unusual phenomenon among pelagic seabirds. We have compared the moult schedules in Cory’s Shearwater colonies located in distinct environments (pelagic vs. coastal) and show that moult–breeding overlap is less extensive on Selvagem Grande, situated in deep oceanic waters, than on Berlenga, situated on the continental shelf. Colony attendance of failed breeders, most of which were moulting, was lower at Selvagem Grande than at Berlenga, which suggests that the feeding areas of birds from the former site are more distant from the colony. Failed breeders started to moult earlier than individuals still raising a chick, and breeding status had a stronger influence on determining the onset of wing-feather moult than colony location. Despite published evidence that internal circannual rhythms and external cues, such as variation in daylength, are important factors regulating moult schedules, it is clear that birds retain a considerable flexibility that allows them to respond to external factors in order to strategically manage time and energy in a way that is thought to maximise their fitness.