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

• Published in: Biological reviews of the Cambridge Philosophical Society Vol. 92; no. 3; pp. 1475 - 1504
• Main Author: Maina, John N.
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.08.2017
• Subjects: Abundance; aerodynamic valving; Aerodynamics; Aerosols; air capillaries; Air flow; airflow; Animal husbandry; Animals; Basement membranes; Birds; Birds - physiology; blood capillaries; Blood vessels; Breathing; Bridges; Capillaries; Capillaries - physiology; Cellular manufacture; cellular protection; Collagen; Connective tissues; Control systems; Control valves; Egg production; Elastin; Fibers; Force-feeding; Gas exchange; lung; Lung - anatomy & histology; Lung - physiology; Lungs; Macrophages; Membranes; Overcrowding; parabronchus; Particulates; Pathogens; Phagocytes; Poultry; Poultry production; Respiration; Respiratory Physiological Phenomena; Respiratory system; Respiratory System - anatomy & histology; Smooth muscle; Structure-function relationships; Valves; Ventilation; Vertebrates; lung; parabronchus; blood capillaries; airflow; cellular protection; aerodynamic valving; air capillaries; birds; gas exchange
• ISSN: 1464-7931; 1469-185X
• DOI: 10.1111/brv.12292

ABSTRACT 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.