Avian Respiratory System Research Articles

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.

Anatomical nomenclature of fossil vertebrates: standardized terms or ‘lingua franca’?

ABSTRACT Whereas the anatomy of birds, domesticated mammals, and humans is described by standardized terminology, the anatomy of most fossil vertebrates is described by nonstandardized terminology. New fossil discoveries increasingly resolve the transitions between these living groups and their fossil outgroups, diminishing morphological differences between them, and vertebrate paleontologists can easily apply more than one system of anatomical terms to such groups. This plurality of systems has led to recent proposals to standardize anatomical terminology for tetrapods, either by applying avian and mammalian anatomical terminology to their respective stem groups (Sauropsida and Synapsida) or by creating an all-encompassing terminology for Tetrapoda from a combination of existing terminologies. The main rationale for implementing standardized anatomical terminology, which requires abandoning competing terminologies, is that it reflects homology and evolutionary descent, eliminates ambiguity, and enhances interdisciplinary communication. The proposed standardized anatomical terminology, however, entails many negative consequences, including reversing character trajectories, misrepresenting complex anatomical transformations and uncertain homologies, and requiring far-reaching terminological conversions. These negative consequences result from increasing the taxonomic scope of standardized anatomical terms that were developed for a specific group, but now: (1) apply to a broader hierarchy of character states; (2) involve additional phylogenetic interpretations or assumptions; and (3) are used for basal, often more generalized conditions. In contrast, traditional non-standardized anatomical terminology, although not strictly phylogenetic, is anatomical ‘lingua franca’ that has been in usage for nearly two centuries and is consistent, ubiquitous, and descriptive.

Spectacularly robust! Tensegrity principle explains the mechanical strength of the avian lung

Among the air-breathing vertebrates, the respiratory system of birds, the lung-air sac system, is remarkably complex and singularly efficient. The most perplexing structural property of the avian lung pertains to its exceptional mechanical strength, especially that of the minuscule terminal respiratory units, the air- and the blood capillaries. In different species of birds, the air capillaries range in diameter from 3 to 20 micro m: the blood capillaries are in all cases relatively smaller. Over and above their capacity to withstand enormous surface tension forces at the air-tissue interface, the air capillaries resist mechanical compression (parabronchial distending pressure) as high as 20 cm H(2)O (2 kPa). The blood capillaries tolerate a pulmonary arterial vascular pressure of 24.1 mmHg (3.2 kPa) and vascular resistance of 22.5 mmHg (3 kPa) without distending. The design of the avian respiratory system fundamentally stems from the rigidity (strength) of the lung. The gas exchanger (the lung) is uncoupled from the ventilator (the air sacs), allowing the lung (the paleopulmonic parabronchi) to be ventilated continuously and unidirectionally by synchronized bellows like action of the air sacs. Since during the ventilation of the lung the air capillaries do not have to be distended (dilated), i.e., surface tension force does not have to be overcome (as would be the case if the lung was compliant), extremely intense subdivision of the exchange tissue was possible. Minuscule terminal respiratory units developed, producing a vast respiratory surface area in a limited lung volume. I make a case that a firm (rigid) rib cage, a lung tightly held by the ribs and the horizontal septum, a lung directly attached to the trunk, specially formed and compactly arranged parabronchi, intertwined atrial muscles, and tightly set air capillaries and blood capillaries form an integrated hierarchy of discrete network system of tension and compression, a tensegrity (tensional integrity) array, which absorbs, transmits, and dissipates stress, stabilizing (strengthening) the lung and its various structural components.

PHYLOGENY OF NEORNITHES

This work serves as a compendium of anatomical resources upon which a companion phylogenetic analysis of Aves and related Theropoda (Avialae) was based (Livezey and Zusi 2006). Following a brief historical overview of avian anatomy and avian systematics, the rich published literature pertinent to these topics is classified chronologically and geographically. The former also was organized with respect to eras of predominant methodologies in avian systematics, with an emphasis on recent paleontological finds bearing importantly on the origins of modern birds (Neornithes). This was followed by an exposition on the theoretical and abstract underpinnings of morphological characterization for purposes of phylogenetic reconstructions (to be published separately), with aspects of analysis for phylogenetic inference (e.g., tactics for employment of currently available software, ordering, criteria for optimization of trees) considered elsewhere.The principal contribution of this exposition is a listing of characters and states manifesting what was inferred to hold promise with respect to phylogenetic or historical signal. In total, 2,954 anatomical characters were defined—2,451 osteological, 256 myological, and 247 miscellaneous—of which 981 (approximately one-third) were multiple-state (i.e., comprised three or more states), the latter including 537 characters treated as ordered. Bibliographic provenance for characters was provided, where possible, but exact equivalence of characters and states among workers was seldom feasible. In many cases, previously published characters were listed on the grounds that these pertained most closely to the structure or complex at hand in the present study, and that such listings provided at least a historical grasp of the magnitude of prior usages of a given character. We also summarized, to the extent feasible, previously published characters for which inclusion in the present work was judged to be unreliable or lacking sufficient clarity.In addition to the descriptions of characters, a limited series of figures are provided, in no small part to ameliorate the challenges posed by new terms and formal anatomical nomenclature. We are adherents to nomenclatural formalism (Livezey and Zusi 2001) in anatomical contexts sensu the ICAAN (International Committee on Avian Anatomical Nomenclature; Baumel 1993). I.e., we consider that characters and states—implicitly proposals of homology—warrant clarity with respect to surrounding text in the same sense that binomial taxa—i.e., as hypotheses of historical lineages—are subject to formal conventions.Finally, literature cited herein is listed, as a work of this kind is impossible without access to the wealth of information and insight provided by such a resource. As this literature is integrated by citation with the descriptions of characters, it is hoped that the bibliography will lessen the challenges posed by a deep, multilingual, and variably technical literature for systematists using these descriptions. The dimension of the character matrix also led us to enclose a CD of the data set in the present work to assist those seeking to improve, append, or refine our efforts.A phylogenetic (cladistic) analysis of these data will appear separately (Livezey and Zusi 2006). Soon thereafter a collaboration with an unparalleled compilation of molecular data (i.e., DNA sequences) and confirmatory paleontological data is planned to conclude with the publication of a total-evidence analysis of avian phylogeny under the auspices of the NSF “Tree of Life” program, one to encompass extant birds (Neornithes), avian relatives from the Mesozoic (outgroups), and nonavialian fossil taxa from the Mesozoic (“deep” outgroups).

Embryonic Effects of Androgen Active Endocrine Disrupting Chemicals on Avian Immune and Reproductive Systems

Embryonic Effects of Androgen Active Endocrine Disrupting Chemicals on Avian Immune and Reproductive Systems

Nymphal development of Xyleus discoideus discoideus (Serville 1831) (Acridoidea, Romaleidae, Romaleinae) in the laboratory

Abstract Nymphal instars of Xyleus discoideus discoideus, a romaleid grasshopper, are described for the first time. The following characters are recorded for each stage: body length, head width, pronotal length, hind femoral length, number of antennomeres, number of longitudinal eye stripes and the morphology of wing pads and external genitalia. Criteria that can be used to distinguish the instars and sexes are identified. Males and females have a 5-instar cycle under laboratory conditions. Females are larger as adults than males and this is linked to a longer nymphal period in females.

Teaching of Practical Anatomy in the University of Veterinary Science

Morphology subjects taught by our department are very important parts of the veterinary medical studies. Functional anatomy, concluded with a final exam, provides knowledge of classical anatomy and is taught for three semesters. The lectures are followed by the plenary sessions where the dissection is done under a camcorder, which shows the students the methods used. Topographical anatomy is taught in the fourth semester – mostly demonstrated on live animals – the visible, palpable structures and the projections of the inner organs on the surface of the body. Introduction to biology summarizes the study of cell biology and also the general knowledge of developmental anatomy. Histology is also given in the second and third semesters, ending with a final exam. However, for the 25 years I have been teaching the anatomy and the subjects taught by our department, I always had the feeling that the students do not pay enough attention or show much appreciation of these studies after the initial enthusiasm. Anatomical knowledge should also be well known during the later year studies at our university. Until recently our teaching program lacked the repetition of systemic anatomical studies that is mostly for applied science. The very recently introduced elective courses, such as radiological anatomy, surgical anatomy, organogenesis and the anatomy of birds are all scheduled for the late evening hours, but the lecture hall are still always full with students of all grades. The enquirers could find the needed anatomical information in special books and atlases until now. However, practising vets say it takes a lot of time and making uncomfortable difficulties to analyse the books. Because of forgetting the details that are less important for the vet's everyday work it can be hard to find solutions for small but urgent problems. That is why we decided to picturise and make a summary in an edition for demonstrating different elements of certain species of animals. The multimedia CD‐ROM was made based on clinical view providing the opportunity for the vet to analysing and studying the part that is the actually subject of his work. After 30 years long break, today there is no graduate or continuing education program without teaching anatomy, which means to give the knowledge to our colleagues applying to their needs also to their everyday work.

Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs

Birds are unique among living vertebrates in possessing pneumaticity of the postcranial skeleton, with invasion of bone by the pulmonary air-sac system. The avian respiratory system includes high-compliance air sacs that ventilate a dorsally fixed, non-expanding parabronchial lung. Caudally positioned abdominal and thoracic air sacs are critical components of the avian aspiration pump, facilitating flow-through ventilation of the lung and near-constant airflow during both inspiration and expiration, highlighting a design optimized for efficient gas exchange. Postcranial skeletal pneumaticity has also been reported in numerous extinct archosaurs including non-avian theropod dinosaurs and Archaeopteryx. However, the relationship between osseous pneumaticity and the evolution of the avian respiratory apparatus has long remained ambiguous. Here we report, on the basis of a comparative analysis of region-specific pneumaticity with extant birds, evidence for cervical and abdominal air-sac systems in non-avian theropods, along with thoracic skeletal prerequisites of an avian-style aspiration pump. The early acquisition of this system among theropods is demonstrated by examination of an exceptional new specimen of Majungatholus atopus, documenting these features in a taxon only distantly related to birds. Taken together, these specializations imply the existence of the basic avian pulmonary Bauplan in basal neotheropods, indicating that flow-through ventilation of the lung is not restricted to birds but is probably a general theropod characteristic.

Nestling provisioning by male and female Yellow-breasted Chats: no relationships between morphology and parental care

Abstract In birds, males and females may benefit by choosing mates based on morphological characteristics correlated with their ability to provide parental care. Our objective was to examine possible relationships between morphological characteristics and the provisioning behavior of male and female Yellow-breasted Chats (Icteria virens). No differences were found in the provisioning behavior of male and female Yellow-breasted Chats. Adult chats provisioned nestlings at higher rates and delivered more biomass at first nests than during later nesting attempts. This indicates that, later in the breeding season, nestling chats may require less energy, perhaps because warmer temperatures lower thermoregulatory costs. No correlations, either positive or negative, between chat morphological characteristics (mass, eye stripe length, tail length, wing chord, tarsus length, and plumage color) and provisioning behavior were noted. Thus, these results do not provide support for either the honest advertisement hypoth...

Metabolic and Ventilatory Acclimatization to Cold Stress in House Sparrows (Passer domesticus)

Passerines that overwinter in temperate climates undergo seasonal acclimatization that is characterized by metabolic adjustments that may include increased basal metabolic rate (BMR) and cold-induced summit metabolism (M(sum)) in winter relative to summer. Metabolic changes must be supported by equivalent changes in oxygen transport. While much is known about the morphology of the avian respiratory system, little is known about respiratory function under extreme cold stress. We examined seasonal variation in BMR, M(sum), and ventilation in seasonally acclimatized house sparrows from Wisconsin. BMR and M(sum) increased significantly in winter compared with summer. In winter, BMR increased 64%, and M(sum) increased 29% over summer values. The 64% increase in winter BMR is the highest recorded for birds. Metabolic expansibility (M(sum)/BMR) was 9.0 in summer and 6.9 in winter birds. The metabolic expansibility of 9.0 in summer is the highest yet recorded for birds. Ventilatory accommodation under helox cold stress was due to changes in breathing frequency (f), tidal volume, and oxygen extraction efficiency in both seasons. However, the only significant difference between summer and winter ventilation measures in helox cold stress was f. Mean f in helox cold stress for winter birds was 1.23 times summer values.

Approach to the dyspneic avian patient

After a description of anatomy and physiology of the avian respiratory system, an approach to the dyspneic patient is discussed. Diagnostics that may be helpful in determining the cause of dyspnea include radiographic imaging, ultrasound, cytology of sinus or tracheal flushes, and endoscopy. Various avian respiratory diseases that may present on an emergency basis are described along with therapeutic options.

Limits on the evolution of tail ornamentation in birds.

In birds, elongated tails are one of the most common and most studied ornaments. However, the tail also has an aerodynamic function, playing a role in turning and slow flight. If a tail is to function as an ornament, then there will be an inevitable conflict between the aerodynamic role and the signaling role. Aerodynamic theory has developed to the point where it is possible to predict the aerodynamic and mechanical consequences of ornamental tails of different sizes and shapes. Tail elongation will influence many different mechanical and aerodynamic parameters. For at least some and possibly all of these parameters, there will be limits that are placed by the bird's anatomy, morphology, or physiology on the extent to which the effect of tail elongation could be tolerated. For example, if a particular tail morphology meant that the power required to fly exceeded the power available from the flight muscles, then the bird would obviously be unable to fly with such a tail. To examine whether these considerations could limit the development of ornamental tails, the effect of long tails of different shapes was examined on three parameters: static balance, lift-to-drag ratio, and the cost of flight. All three of these parameters were found to limit the range of possible tail morphologies that could be developed by birds. These limits were most acute for small birds, which may not be able to operate with a long tail of any shape. Slightly larger birds would be able to develop elongated streamers and forked tails but not pintails or wedge-shaped tails. Medium to large birds are less constrained and could develop a much wider range of tails than small birds, but there will always be limits to the sizes of tail ornament that could be developed. Thus the physical consequences of ornamentation on ecology and behavior are likely to be responsible for some of the patterns of ornamentation observed in nature.

Developmental dynamics of the bronchial (airway) and air sac systems of the avian respiratory system from day�3 to day 26 of life: a scanning electron microscopic study of the domestic fowl, Gallus gallus variant domesticus

The lung buds were first conspicuous on day 3 of embryogenesis. They fused on day 4 and the common growth divided into left and right primordial lungs on day 5. Progressively, the lungs elongated, diverged, and advanced towards the respective dorsolateral aspects of the body wall, reaching their definitive topographical locations in the coelomic cavity on day 6. On day 7, they rotated, attached onto the ribs, gradually started to slide into them, and were deeply inserted by day 8. The primary bronchus (PB) first appeared as a solid cord of epithelial cells (day 4) that successively canalized as it invaded the surrounding mesenchyme, extending along the proximal-distal axis of the lung. From day 8, the secondary bronchi (SB) begun to sprout from the PB in a craniocaudal sequence. On day 9, the parabronchi (PR) started to bud from the SB, projecting into the adjacent mesenchyme. They commenced to canalize on day 10 and greatly increased in length, number, and diameter. By day 13, the PR had anastomosed profusely and totally masked the SB. The luminal surface of the PR was lined by a columnar epithelium from which the atria (day 15), infundibulae (day 16), and air capillaries (ACs) (day 18) developed. At hatching (day 21), the ACs were well developed and had anastomosed profusely with the blood capillaries. Of the air sacs (ASs), the abdominal ones appeared earliest (day 5) followed by the cervical ones on day 6. In quick succession, the other ASs were well formed by day 10. After hatching, no further consequential structures formed: only shifts in topographical locations and an increase in size and number occurred. Morphogenetically, the avian respiratory system differs from the mammalian one in certain key aspects: besides the ASs that are unique to it, the lung is exceptionally complex in structure and is essentially mature at the end of the embryonic life.

Why Parental Sex Ratio Manipulation is Rare in Higher Vertebrates (Invited Article)

The debate over adaptive parental sex ratio adjustment in higher vertebrates appears neither to be resolvable by the current approach, nor does it necessarily make sense. It rests on the a priori supposition of parental manipulation, which is questioned here from first principle. It is considered an unlikely biological hypothesis if we extend our perspective to gametic and offspring optimal strategies, and to the potential mechanisms existing in the avian and mammalian reproductive systems. Evenness of primary sex ratios is expected to be optimal from the gametic point of view and is supposed here to be the more likely evolutionary outcome. Also, manipulations by sex‐selective offspring mortality is argued to be unlikely as usually the benefits will be surpassed by the costs incurred. Furthermore, parents can adjust behavioural and energetic investment patterns to their offspring sex (ratio), thereby minimizing any costs of sex ratio control inability. Slight biases in offspring sex ratios are then viewed as resulting from physiological limitations ultimately relating to sex differences in embryonic development. Contrary to recent attempts to understand higher vertebrate sex ratio variation by further refinement of functional models (of parental optima) and data analysis, Bayesian logic precludes those approaches to gain useful new insights. To prove the basic assumption of parental manipulation, apart from defining gametic and offspring optima, the emphasis should lie on identifying control mechanisms by experimental verification.

Sound radiation patterns in Nightingale (Luscinia megarhynchos) songs

Songs of a Nightingale (Luscinia megarhynchos) were recorded in front of the bird (on-axis) and simultaneously at various off-axis angles. The pattern of sound radiation in the horizontal plane around the singing bird proved to be clearly directional with a median front-back difference (0°–180°) of 4.6 dB. This deviation from omnidirectionality seems to be an inevitable result of the bird's anatomy (i. e. sound shadow effects of the head and body) but some bird species may counteract the directionality of their songs by means of behaviour. Moreover, the directional song radiation pattern might be used to direct songs towards addressees of the signals.

An improved breeding method for solitarious locusts

AbstractIn order to unravel the physiological, endocrine, and behavioral differences between gregarious and solitarious forms of the desert locust, Schistocerca gregaria (Forsk.) (Orthoptera, Acrididae), a constant supply of rather large numbers of solitary individuals has to be guaranteed. This represents a bottleneck, mainly because of the intensity of the labor involved and limited laboratory accommodation. The method we describe here substantially reduces the space and manpower needed. The survival rate we obtained in the solitarised population was relatively high, reaching about 55%. The optimal rearing temperature proved to be 32–36 °C. Cabbage leaves and oat flakes sufficed for feeding all year round. Special racks have been designed that enable high density stacking and easy handling. The solitarisation process was monitored over ten consecutive generations. Changes in morphometrics, eye stripes, color, and behavior were recorded, of which only morphometrics, temperature related development, and mortality are discussed. A shift towards the solitarious phase was recorded, with clear differences between gregarious, 1st generation and 7th to 10th generation solitarious locusts.

Review of Wound Management in Raptors

Birds of prey encounter many injuries that make treatment a challenging process. These include electrocution, trauma-associated cuts and abrasions, gunshot wounds, barbed wire and leghold trap ensnarement, puncture wounds, and damage from inappropriate housing and husbandry. The mechanism of wound healing is similar to that seen in mammals, with a continuous progression through the phases of inflammation, proliferation, and remodeling. Healing by primary closure (suturing) is generally preferable to healing by secondary intention, though the latter is more common in raptors because of the delayed presentation of most wounds. Debridement and lavage, with chlorhexidine at a 0.05% solution being considered to provide optimal results, are required for all wounds. Many topical medications are used to manage open wounds in raptors, including recently developed wound-healing stimulants. Bandage materials used are the same as those used for other species, though the type of bandage varies according to the uniqueness of avian anatomy. Specific injuries such as bumblefoot, degloving, frostbite, digital amputation, and crop laceration may require special consideration.

Differential Avian Skeletal Part Distribution: Explaining the Abundance of Wings

An abundance of wings relative to other skeletal parts has been observed in avifaunal assemblages from many different types of archaeological sites from numerous locations around the world and of various time periods. Both cultural and post-depositional hypotheses have been proposed to explain this pattern. One of the most powerful explanations to account for this phenomenon is differential survival of avian elements due to bone density. Although bone density has not been systematically measured for all types of birds, I test this hypothesis using predictions derived from observations about the functional anatomy of birds using archaeological data from numerous sites in the Pacific Northwest Coast (U.S.A.). I conclude that the density hypothesis is not supported at these sites, and that other hypotheses must be examined further.

Higher-level systematic analysis of birds: current problems and possible solutions.

Avian systematics has a rich history, as evolutionary biologists have long been interested in this conspicuous and diverse group of vertebrates. Many prominent scientists, and evolutionary biologists in particular, have focused their efforts on birds. Perhaps no other group of vertebrates is so well studied. Yet, despite the attention paid to this group, much about the history of the class Aves remains controversial, both with respect to the origin of birds and the history since that origin. This puts avian systematists in a unique position, with so much information available and so many unanswered questions to pursue. The fact that avian ordinal relationships are still the center of much controversy speaks to the difficulty of the problem. While many prominent morphologists have worked on avian relationships, relatively few morphological studies have identified characters with informative variation for interordinal relationships. Molecular data offer the hope for phylogenetic information not present (or not discovered) in avian anatomy. Since the first study of avian proteins for the purposes of systematics (Sibley, 1960), several prominent molecular systematists have devoted tremendous time and resources to solving the problems of avian relationships using molecular characters (see Barrowclough, 1992 and Sheldon and Bledsoe, 1993 and references therein). So far, their efforts have not produced adequate resolution, at least not in the minds of most practicing systematists. Here, we first outline what we think we do know about higher order avian systematics and discuss some specific cases of molecular data applied to this question. Next, we consider some of the problems which may be blocking a clearer understanding of avian relationships. We then go on to offer some new directions for systematists working on this difficult group.

In vivo magnetic resonance imaging of the reproductive organs in a passerine bird species

For researchers working on the reproductive anatomy of birds, the standard tool has been the scalpel. We demonstrate that magnetic resonance imaging (MRI) allows us to study non‐invasively the testes and ovaries of small birds. Thus, repeated measurements of the same individual can be obtained at different life‐history stages or before and after experimental treatment with a minimum of harm done to the birds. We present cross‐sectional images of male and female Garden Warblers Sylvia borin at different stages of their gonadal maturation cycle to illustrate the high resolution that can be achieved through MRI. Volumetric analyses enabled us to determine the total testicular volume with high accuracy.