Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina

Background

Living birds possess a unique heterogeneous pulmonary system composed of a rigid, dorsally-anchored lung and several compliant air sacs that operate as bellows, driving inspired air through the lung. Evidence from the fossil record for the origin and evolution of this system is extremely limited, because lungs do not fossilize and because the bellow-like air sacs in living birds only rarely penetrate (pneumatize) skeletal bone and thus leave a record of their presence.

Methodology/Principal Findings

We describe a new predatory dinosaur from Upper Cretaceous rocks in Argentina, Aerosteon riocoloradensis gen. et sp. nov., that exhibits extreme pneumatization of skeletal bone, including pneumatic hollowing of the furcula and ilium. In living birds, these two bones are pneumatized by diverticulae of air sacs (clavicular, abdominal) that are involved in pulmonary ventilation. We also describe several pneumatized gastralia (“stomach ribs”), which suggest that diverticulae of the air sac system were present in surface tissues of the thorax.

Conclusions/Significance

We present a four-phase model for the evolution of avian air sacs and costosternal-driven lung ventilation based on the known fossil record of theropod dinosaurs and osteological correlates in extant birds:(1) Phase I—Elaboration of paraxial cervical air sacs in basal theropods no later than the earliest Late Triassic.(2) Phase II—Differentiation of avian ventilatory air sacs, including both cranial (clavicular air sac) and caudal (abdominal air sac) divisions, in basal tetanurans during the Jurassic. A heterogeneous respiratory tract with compliant air sacs, in turn, suggests the presence of rigid, dorsally attached lungs with flow-through ventilation.(3) Phase III—Evolution of a primitive costosternal pump in maniraptoriform theropods before the close of the Jurassic.(4) Phase IV—Evolution of an advanced costosternal pump in maniraptoran theropods before the close of the Jurassic.In addition, we conclude:(5) The advent of avian unidirectional lung ventilation is not possible to pinpoint, as osteological correlates have yet to be identified for uni- or bidirectional lung ventilation.(6) The origin and evolution of avian air sacs may have been driven by one or more of the following three factors: flow-through lung ventilation, locomotory balance, and/or thermal regulation.     

The theropod furcula

The furcula is a structure formed by the midline fusion of the clavicles. This is the element which is unique to theropods and is important for understanding the link between birds and other theropods. New specimens from basal theropods suggest that the furcula appeared very early in theropod history. We review furcula development, function, and morphology, as well as the anatomical terminology applied to it. Furcular morphology is highly variable in crown‐group avians but is rather conserved among nonavian theropods. Here we review, or describe for the first time, the furculae in many nonavian theropods. Furculae occur in nearly all major clades of theropods, as shown by new theropod specimens from the Early Cretaceous of China and a close inspection of previously collected specimens. Informative phylogenetic characters pertaining to the furcula occur throughout Theropoda, though care should betake to consider taphonomic effects when describing furcular morphology. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Mesenchymal control of branching pattern in the fetal mouse lung

The effect of mesenchyme on specialization of respiratory epithelium in the fetal mouse was tested in organ cultures. Heterologous combinations were made between respiratory and non-respiratory lung epithelia and the corresponding mesenchymes. Isolated terminal respiratory buds of fetal mouse lungs were recombined with mesenchyme from chick lung parabronchi, mouse trachea or from the avascular, non-respiratory air sacs of chick lungs. Isolated non-branching chick air sacs were combined with mouse terminal bud mesenchyme or mesenchyme from the respiratory branches of chick lungs. Air sac epithelia branched in a pattern characteristic of the chick lung when combined with chick respiratory mesenchyme and in a pattern characteristic of mouse lung when combined with mouse terminal bud mesenchyme. Mouse terminal bud epithelia did not branch with either mouse tracheal mesenchyme or chick air sac mesenchyme but branched in a chick pattern with chick parabronchial mesenchyme. Electron microscopic examination of the cultures showed that all chick air sac epithelial cultures failed to produce surfactant (lamellar bodies) even when they branched. Control cultures of mouse terminal buds contained large numbers of lamellar bodies; mesenchyme which suppressed branching reduced the number of lamellar bodies to only a few in a small proportion of the cells. Culture medium supplemented with growth factors and hormones increased the number of lamellar bodies in heterologous mouse combinations but did not bring the number to control levels. Supplemented medium had no effect on lamellar body production by chick air sac epithelium. The results indicate that branching pattern is determined by the mesenchyme surrounding the epithelial primordium. However, the capacity to synthesize surfactant is determined by the source of the epithelium; mesenchyme may control the degree of expression but not the absolute presence or absence of the differentiated condition.     

Postcranial pneumaticity: an evaluation of soft-tissue influences on the postcranial skeleton and the reconstruction of pulmonary anatomy in archosaurs

Postcranial pneumaticity has been reported in numerous extinct sauropsid groups including pterosaurs, birds, saurischian dinosaurs, and, most recently, both crurotarsan and basal archosauriform taxa. By comparison with extant birds, pneumatic features in fossils have formed the basis for anatomical inferences concerning pulmonary structure and function, in addition to higher-level inferences related to growth, metabolic rate, and thermoregulation. In this study, gross dissection, vascular and pulmonary injection, and serial sectioning were employed to assess the manner in which different soft tissues impart their signature on the axial skeleton in a sample of birds, crocodylians, and lizards. Results from this study indicate that only cortical foramina or communicating fossae connected with large internal chambers are reliable and consistent indicators of pneumatic invasion of bone. As both vasculature and pneumatic diverticula may produce foramina of similar sizes and shapes, cortical features alone do not necessarily indicate pneumaticity. Noncommunicating (blind) vertebral fossae prove least useful, as these structures are associated with many different soft-tissue systems. This Pneumaticity Profile (PP) was used to evaluate the major clades of extinct archosauriform taxa with purported postcranial pneumaticity. Unambiguous indicators of pneumaticity are present only in certain ornithodiran archosaurs (e.g., sauropod and theropod dinosaurs, pterosaurs). In contrast, the basal archosauriform Erythrosuchus africanus and other nonornithodiran archosaurs (e.g., parasuchians) fail to satisfy morphological criteria of the PP, namely, that internal cavities are absent within bone, even though blind fossae and/or cortical foramina are present on vertebral neural arches. An examination of regional pneumaticity in extant avians reveals remarkably consistent patterns of diverticular invasion of bone, and thus provides increased resolution for inferring specific components of the pulmonary air sac system in their nonavian theropod ancestors. By comparison with well-preserved exemplars from within Neotheropoda (e.g., Abelisauridae, Allosauroidea), the following pattern emerges: pneumaticity of cervical vertebrae and ribs suggests pneumatization by lateral vertebral diverticula of a cervical air sac system, with sacral pneumaticity indicating the presence of caudally expanding air sacs and/or diverticula. The identification of postcranial pneumaticity in extinct taxa minimally forms the basis for inferring a heterogeneous pulmonary system with distinct exchange and nonexchange (i.e., air sacs) regions. Combined with inferences supporting a rigid, dorsally fixed lung, osteological indicators of cervical and abdominal air sacs highlight the fundamental layout of a flow-through pulmonary apparatus in nonavian theropods.     

Pivotal debates and controversies on the structure and function of the avian respiratory system: setting the record straight

Among the extant air‐breathing vertebrates, the avian respiratory system is structurally the most complex and functionally the most efficient gas exchanger. Having been investigated for over four centuries, some aspects of its biology have been extremely challenging and highly contentious and others still remain unresolved. Here, while assessing the most recent findings, four notable aspects of the structure and function of the avian respiratory system are examined critically to highlight the questions, speculations, controversies and debates that have arisen from past research. The innovative techniques and experiments that were performed to answer particular research questions are emphasised. The features that are outlined here concern the arrangement of the airways, the path followed by the inspired air, structural features of the lung and the air and blood capillaries, and the level of cellular defence in the avian respiratory system. Hitherto, based on association with the proven efficiency of naturally evolved and human‐made counter‐current exchange systems rather than on definite experimental evidence, a counter‐current gas exchange system was suggested to exist in the avian respiratory system and was used to explain its exceptional efficiency. However, by means of an elegant experiment in which the direction of the air‐flow in the lung was reversed, a cross‐current system was shown to be in operation instead. Studies of the arrangement of the airways and the blood vessels corroborated the existence of a cross‐current system in the avian lung. While the avian respiratory system is ventilated tidally, like most other invaginated gas exchangers, the lung, specifically the paleopulmonic parabronchi, is ventilated unidirectionally and continuously in a caudocranial (back‐to‐front) direction by synchronized actions of the air sacs. The path followed by the inspired air in the lung–air sac system is now known to be controlled by a mechanism of aerodynamic valving and not by anatomical valves or sphincters, as was previously supposed. The structural strength of the air and blood capillaries is derived from: the interdependence between the air and blood capillaries; a tethering effect between the closely entwined respiratory units; the presence of epithelial–epithelial cell connections (retinacula or cross‐bridges) that join the blood capillaries while separating the air capillaries; the abundance and intricate arrangement of the connective tissue elements, i.e. collagen, elastin, and smooth muscle fibres; the presence of type‐IV collagen, especially in the basement membranes of the blood–gas barrier and the epithelial–epithelial cell connections; and a putative tensegrity state in the lung. Notwithstanding the paucity of free surface pulmonary macrophages, the respiratory surface of the avian lung is well protected from pathogens and particulates by an assortment of highly efficient phagocytic cells. In commercial poultry production, instead of weak pulmonary cellular defence, stressful husbandry practices such as overcrowding, force‐feeding, and intense genetic manipulation for rapid weight gain and egg production may account for the reported susceptibility of birds to aerosol‐transmitted diseases.     

白枕鹤的呼吸系统及其生态适应

白枕鹤的呼吸系统由喉头、气管、鸣管、肺及气囊组成。喉头有淋巴小结分布。气管在龙骨突起内盘旋,并随年龄而增长,软骨环逐渐骨化。鸣管由左右两个支气管特化而成,呈膜状扁管入肺。肺的长度约占躯干的1/2。气囊几遍布全身,高度发达。整个呼吸系统的结构,与其高空飞翔生活相适应。     

Dual functions for LTBP in lung development: LTBP‐4 independently modulates elastogenesis and TGF‐β activity

The latent TGF‐β binding proteins (LTBP) ‐1, ‐3, and ‐4 are extracellular proteins that assist in the secretion and localization of latent TGF‐β. The null mutation of LTBP‐4S in mice causes defects in the differentiation of terminal air‐sacs, fragmented elastin, and colon carcinomas. We investigated lung development from embryonic day 14.5 (E14.5) to day 7 after birth (P7) in order to determine when the defects in elastin organization initiate and to further examine the relation of TGF‐β signaling levels and air‐sac septation in Ltbp4S?/? lungs. We found that defects in elastogenesis are visible as early as E14.5 and are maintained in the alveolar walls, in blood vessel media, and subjacent airway epithelium. The air‐sac septation defect was associated with excessive TGF‐β signaling and was reversed by lowering TGF‐β2 levels. Thus, the phenotype is not directly reflective of a change in TGF‐β1, the only TGF‐β isoform known to complex with LTBP‐4. Reversal of the air‐sac septation defect was not associated with normalization of the elastogenesis indicating two separate functions of LTBP‐4 as a regulator of elastic fiber assembly and TGF‐β levels in lungs. J. Cell. Physiol. 219: 14–22, 2009. © 2008 Wiley‐Liss, Inc.     

Avian cholera in a southern giant petrel (Macronectes giganteus) from Antarctica

A southern giant petrel (Macronectes giganteus) was found dead at Potter Peninsula, King George Island, South Shetland, Antarctica. The adult male was discovered approximately 48 hr after death. Macroscopic and microscopic lesions were compatible with avian cholera and the bacterium Pasteurella multocida subsp. gallicida, serotype A1 was isolated from lung, heart, liver, pericardial sac, and air sacs. In addition, Escherichia coli was isolated from pericardial sac and air sacs. This is the first known report of avian cholera in a southern giant petrel in Antarctica.     

Loss of air sacs improved hominin speech abilities

In this paper, the acoustic-perceptual effects of air sacs are investigated. Using an adaptive hearing experiment, it is shown that air sacs reduce the perceptual effect of vowel-like articulations. Air sacs are a feature of the vocal tract of all great apes, except humans. Because the presence or absence of air sacs is correlated with the anatomy of the hyoid bone, a probable minimum and maximum date of the loss of air sacs can be estimated from fossil hyoid bones. Australopithecus afarensis still had air sacs about 3.3 Ma, while Homo heidelbergensis, some 600 000 years ago and Homo neandethalensis some 60 000 years ago, did no longer. The reduced distinctiveness of articulations produced with an air sac is in line with the hypothesis that air sacs were selected against because of the evolution of complex vocal communication. This relation between complex vocal communication and fossil evidence may help to get a firmer estimate of when speech first evolved.     

Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone

Among the air-breathing vertebrates, the avian respiratory apparatus, the lung-air sac system, is the most structurally complex and functionally efficient. After intricate morphogenesis, elaborate pulmonary vascular and airway (bronchial) architectures are formed. The crosscurrent, countercurrent, and multicapillary serial arterialization systems represent outstanding operational designs. The arrangement between the conduits of air and blood allows the respiratory media to be transported optimally in adequate measures and rates and to be exposed to each other over an extensive respiratory surface while separated by an extremely thin blood-gas barrier. As a consequence, the diffusing capacity (conductance) of the avian lung for oxygen is remarkably efficient. The foremost adaptive refinements are: (1) rigidity of the lung which allows intense subdivision of the exchange tissue (parenchyma) leading to formation of very small terminal respiratory units and consequently a vast respiratory surface; (2) a thin blood-gas barrier enabled by confinement of the pneumocytes (especially the type II cells) and the connective tissue elements to the atria and infundibulae, i.e. away from the respiratory surface of the air capillaries; (3) physical separation (uncoupling) of the lung (the gas exchanger) from the air sacs (the mechanical ventilators), permitting continuous and unidirectional ventilation of the lung. Among others, these features have created an incredibly efficient gas exchanger that supports the highly aerobic lifestyles and great metabolic capacities characteristic of birds. Interestingly, despite remarkable morphological heterogeneity in the gas exchangers of extant vertebrates at maturity, the processes involved in their formation and development are very similar. Transformation of one lung type to another is clearly conceivable, especially at lower levels of specialization. The crocodilian (reptilian) multicameral lung type represents a Bauplan from which the respiratory organs of nonavian theropod dinosaurs and the lung-air sac system of birds appear to have evolved. However, many fundamental aspects of the evolution, development, and even the structure and function of the avian respiratory system still remain uncertain.     

A review of cetacean lung morphology and mechanics

Cetaceans possess diverse adaptations in respiratory structure and mechanics that are highly specialized for an array of surfacing and diving behaviors. Some of these adaptations and air management strategies are still not completely understood despite over a century of study. We have compiled the historical and contemporary knowledge of cetacean lung anatomy and mechanics in regards to normal lung function during ventilation and air management while diving. New techniques are emerging utilizing pulmonary mechanics to measure lung function in live cetaceans. Given the diversity of respiratory adaptations in cetaceans, interpretations of these results should consider species‐specific anatomy, mechanics, and behavior. J. Morphol. 274:1425–1440, 2013. © 2013 Wiley Periodicals, Inc.     

Axial and appendicular pneumaticity in Archaeopteryx

From the time of its discovery in 1860 to this day Archaeopteryx has been essential to our understanding of avian evolution. Despite the great diversity of plesiomorphic avialan (sensu Gauthier 1986) taxa discovered within the last decade, Archaeopteryx remains the most basal avialan taxon. A very unusual feature of extant birds is their lung structure, in which air diverticulae penetrate the bones. This has previously been reported in Archaeopteryx as well, in the cervical vertebrae of the Berlin specimen and in an anterior thoracal vertebra of the Eichstätt specimen. This indicates the presence of a cervical air sac. We show that the London specimen also has pneumatized anterior thoracal vertebrae, and, thus, that this feature was present in the most archaic avialans, as the London and Eichstätt specimens are different species. Furthermore, the pelvis of the London specimen shows clear signs of the presence of an abdominal air sac, indicating that at least two of the five air sacs present in modern birds were also present in Archaeopteryx. Evidence of pubic pneumaticity was also found in the same position in some extant ratites.     

The functions of laryngeal air sacs in primates: a new hypothesis

A possible function of laryngeal air sacs in apes and gibbons was investigated by examining the relationships between air sac distribution, call rate, call duration and body weight in a phylogenetic context. The results suggest that lack of sacs in the smaller gibbons and in humans is a derived feature. Call parameters in primates, such as rate and duration, scaled to resting breathing rate (and therefore to body weight) only in species without air sacs, which appear to modify these relationships. Apes and larger gibbons may be able to produce fast extended call sequences without the risk of hyperventilating because they can re-breathe exhaled air from their air sacs. Humans may have lost air sacs during their evolutionary history because they are able to modify their speech breathing patterns and so reduce any tendency to hyperventilate.     

Estimating body weight and habitat type from extinct avian and avian‐like theropod footprints

The relationship between body weight and footprint area of modern avians was derived and used to estimate the body weights of non‐avian theropods taxa from the Triassic to Cretaceous and extinct avian taxa from the Cretaceous periods. Geometric information, such as the area and shape of fossil tracks of extinct avians and non‐avian theropods, was used to estimate body weight and habitat type. The percentage prediction and standard error of estimates indicated that the body weight estimated from track area is comparable with body weight estimated from body fossils bones. Therefore, this approach is useful when the fossilized track record is richer than the fossilized skeletal record. The data sets for avians and reptiles were combined and used to derive a body weight–area relationship that may be applicable to a broader range of organisms, such as plantigrade quadrupeds and digitigrade bipeds. Additionally, scatter plots of the relationship between habitat type and footprint shape of modern avians were used to infer the habitat type of extinct avians. This finding suggests that the pes of animals, living in areas characterized by fluctuating water levels, and under conditions facilitating the preservation of footprints, were similar in form to those of extant semi‐aquatic avians.     

The vocal sac of Hylodidae (Amphibia,Anura): Phylogenetic and functional implications of a unique morphology

Anuran vocal sacs are elastic chambers that recycle exhaled air during vocalizations and are present in males of most species of frogs. Most knowledge of the diversity of vocal sacs relates to external morphology; detailed information on internal anatomy is available for few groups of frogs. Frogs of the family Hylodidae, which is endemic to the Atlantic Forest of Brazil and adjacent Argentina and Paraguay, have three patterns of vocal sac morphology—that is, single, subgular; paired, lateral; and absent. The submandibular musculature and structure of the vocal sac mucosa (the internal wall of the vocal sac) of exemplar species of this family and relatives were studied. In contrast to previous accounts, we found that all species of Crossodactylus and Hylodes possess paired, lateral vocal sacs, with the internal mucosa of each sac being separate from the contralateral one. Unlike all other frogs for which data are available, the mucosa of the vocal sacs in these genera is not supported externally by the mm. intermandibularis and interhyoideus . Rather, the vocal sac mucosa projects through the musculature and is free in the submandibular lymphatic sac. The presence of paired, lateral vocal sacs, the internal separation of the sac mucosae, and their projection through the m. interhyoideus are synapomorphies of the family. Furthermore, the specific configuration of the m. interhyoideus allows asymmetric inflation of paired vocal sacs, a feature only reported in species of these diurnal, stream‐dwelling frogs.     

Respiratory surface areas of an air-breathing siluroid fish Saccobranchus (Heteropneustes) fossilis in relation to body size

The surface area of the gills, air sacs and skin have been measured in specimens of different body size and their relationship to body weight fits the equation: area= aW^b . The slopes ( b ) of the double logarithmic plots are 0.746 (gills), 0.662 (air sacs) and 0.684 (skin). The gills are poorly developed and their average weight specific area is less than figures obtained for sluggish marine fishes. The skin has an area about 70% of the total respiratory surfaces (gills+air sac+skin). Nevertheless the greater thickness of the skin leads to a smaller diffusing capacity of the tissue barrier ( D_t ) as compared with the gills and air sac. The air sac area for each ml of air that it contains is about 10.5 cm² which is much lower than figures obtained for lungs of other air-breathing fish and for tetrapods.     

The mucous covering of fecal sacs prevents birds from infection with enteric bacteria

Nestlings of many bird species produce fecal sacs, excrements encapsulated within a mucous covering. Although it facilitates parents' removal of feces from nests, which would improve hygienic conditions for developing nestlings, no functional (i.e. adaptive) explanation of fecal sac production has been previously investigated. We propose that the mucous covering would isolate enteric pathogenic bacteria, thereby preventing contamination of nestlings and parents. This antimicrobial hypothesis therefore predicts that density of bacteria would be drastically reduced from the inside to the outside of nestlings' droppings, and that the fecal sac covering would inhibit other bacterial grow. We tested these predictions by means of culturing bacteria obtained from different parts of the sac and inhibition tests. In accordance with the hypothesis, bacterial loads of the outside of fecal sacs were significantly lower than those estimated from the inside of the covering. In addition, we did not find evidence of antimicrobial activity of the covering, which suggests that the hypothesized bacterial isolation function is accomplished by a physical rather than a chemical protection. Bacterial density of the liquid that permeates out after 23 min does not differ with that estimated for the inside of the sac, suggesting short‐term effects of fecal sacs as bacterial barrier. These findings highlight the major role of bacterial infections as a selective pressure for explaining the evolution of traits that, as the covering of fecal sacs, facilitate nest sanitation in this group of animals.     

四倍体双穗雀稗兼性无孢子生殖的研究

研究了四倍体双穗雀稗(Paspalum distichum L)无孢子生殖胚囊、胚胎发育以及假受精特点。当其大孢子母细胞发育至四分体阶段时,大多数情况下会发生四分体退化,同时有多个特化珠心细胞发育为1—3个无孢子生殖胚囊的现象。成熟无孢子生殖胚囊一般3核,包括1个卵细胞和2个极核。卵细胞在抽穗前就能自发分裂形成原胚团,而极核则在抽穗和传粉后参与假受精形成胚乳。当胚珠内存在多个无孢子生殖胚囊时,只是靠近珠孔端的1个无孢子生殖胚囊内的极核与精核结合,而其它的并不参与。种子成熟后出现很低频率的二胚苗。此外,还能观察到少量的有性生殖胚囊的发育以及有性生殖胚囊和无孢子生殖胚囊在同一胚珠中的发育现象,因此判断该类群为兼性无孢子生殖体。     

The evolution of endothermy in terrestrial vertebrates: Who? When? Why?

Avian and mammalian endothermy results from elevated rates of resting, or routine, metabolism and enables these animals to maintain high and stable body temperatures in the face of variable ambient temperatures. Endothermy is also associated with enhanced stamina and elevated capacity for aerobic metabolism during periods of prolonged activity. These attributes of birds and mammals have greatly contributed to their widespread distribution and ecological success. Unfortunately, since few anatomical/physiological attributes linked to endothermy are preserved in fossils, the origin of endothermy among the ancestors of mammals and birds has long remained obscure. Two recent approaches provide new insight into the metabolic physiology of extinct forms. One addresses chronic (resting) metabolic rates and emphasizes the presence of nasal respiratory turbinates in virtually all extant endotherms. These structures are associated with recovery of respiratory heat and moisture in animals with high resting metabolic rates. The fossil record of nonmammalian synapsids suggests that at least two Late Permian lineages possessed incipient respiratory turbinates. In contrast, these structures appear to have been absent in dinosaurs and nonornithurine birds. Instead, nasal morphology suggests that in the avian lineage, respiratory turbinates first appeared in Cretaceous ornithurines. The other approach addresses the capacity for maximal aerobic activity and examines lung structure and ventilatory mechanisms. There is no positive evidence to support the reconstruction of a derived, avian-like parabronchial lung/air sac system in dinosaurs or nonornithurine birds. Dinosaur lungs were likely heterogenous, multicameral septate lungs with conventional, tidal ventilation, although evidence from some theropods suggests that at least this group may have had a hepatic piston mechanism of supplementary lung ventilation. This suggests that dinosaurs and nonornithurine birds generally lacked the capacity for high, avian-like levels of sustained activity, although the aerobic capacity of theropods may have exceeded that of extant ectotherms. The avian parabronchial lung/air sac system appears to be an attribute limited to ornithurine birds.     

Spectrographic analysis of laryngeal air sac resonance in rhesus monkey.

Laryngeal air sacs are circular out-pocketings, located in the hyoid bone with their ostium in the midline of the anterior part of the larynx. From previous cadaver studies of the rhesus monkey it was deduced that the function of the air sac is to act as a resonating chamber. The present study was designed to test this hypothesis. Recordings were made of three rhesus monkeys before and after surgical removal of the air sac. Spectrographic analysis of the monkeys' vocalizations indicated that differences in formant frequency characteristics between pre-and post-surgical recordings were negligible. This finding suggests that the laryngeal air sac does not play an important role in the resonant properties of the monkeys' vocal tracts.