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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\u2010made counter\u2010current exchange systems rather than on definite experimental evidence, a counter\u2010current 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\u2010flow in the lung was reversed, a cross\u2010current 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\u2010current 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\u2010to\u2010front) direction by synchronized actions of the air sacs. The path followed by the inspired air in the lung\u2013air 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\u2013epithelial cell connections (retinacula or cross\u2010bridges) 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\u2010<jats:styled-content style=\"fixed-case\">IV<\/jats:styled-content>collagen, especially in the basement membranes of the blood\u2013gas barrier and the epithelial\u2013epithelial 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\u2010feeding, and intense genetic manipulation for rapid weight gain and egg production may account for the reported susceptibility of birds to aerosol\u2010transmitted diseases.<\/jats:p>","DOI":"10.1111\/brv.12292","type":"journal-article","created":{"date-parts":[[2016,7,28]],"date-time":"2016-07-28T09:44:09Z","timestamp":1469699049000},"page":"1475-1504","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["Pivotal debates and controversies on the structure and function of the avian respiratory system: setting the record straight"],"prefix":"10.1111","volume":"92","author":[{"given":"John N.","family":"Maina","sequence":"first","affiliation":[{"name":"Department of Zoology University of Johannesburg P.O. 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