Lungs and gas bladders: Morphological insights

Abstract

This paper summarizes the main morphological tracts exhibited by lungs and gas bladders in fishes. The origin and organ location, the presence of a glottal region, the inner architecture, the characteristics of the exchange barrier and the presence of pulmonary arteries have been reviewed in the two types of air-breathing organs. With the exception of the dorsal (bladders) or ventral (lungs) origin from the posterior pharynx, none of the morphological traits analyzed can be considered specific for either lungs or gas bladders. This is exemplified by analysis of the morphology of the lung of the Dipnoii and Polypteriformes and of the bladder of the Lepisosteiformes. All of them are obligate air-breathers and show a lung-like (pulmonoid) air-breathing organ. However, while the lungfish lung and the bladder of the Lepisosteiformes occupy a dorsal position and are highly trabeculated, the polypterid lung occupies a ventral position and shows a smooth inner surface. Structural and ultrastructural differences are also highlighted. Noticeably, a large part of the inner surface area of the lung of the Australian lungfish is covered by a ciliated epithelium. A restricted respiratory surface area may help to explain the incapability of this species to aestivate. The respiratory bladder of basal teleosts displays a more complex morphology than that observed in more primitive species. The bladder of basal teleosts may appear divided into respiratory and non-respiratory portions, exhibit intricate shapes, invade adjacent structures and gain additional functions. The increase in morphological and functional complexity appears to prelude the loss of the respiratory functions.

Introduction

Air breathing in fishes is often taken as an evolutionary curiosity that comes as a surprise to many non-specialized researches and amazes to the general public. However, the capacity of air-breathing constitutes a major milestone in vertebrate evolution: it enabled land colonization and the appearance of the tetrapods. Noticeably, fish air breathing cannot be considered a mere step in mammal evolution. Extant species have adopted air breathing to such an extent that many of them suffer or even die when forced to make extended submersions. Other species, such as lungfishes, become exclusive air breathers for long periods of time (e.g., Graham, 1997; Graham et al., 2011).

The entire list of fishes known to (or suspected to) breath air has been provided in an early work (Graham, 1997). The original list appears to be incomplete but it includes up to 374 species of bony fish grouped into 49 families, with one or several members of each family showing this characteristic. Air-breathing species are distributed over a wide range of ecological niches, show variable dependence on aerial oxygen and may be able to travel over land in search of new habitats or food (Liem, 1989; Sayer and Davenport, 1991; Graham, 1997). This behavioral diversity is also reflected in the characteristics of the air breathing organs (ABO). Primitive species rely on saccular organs such as lungs or respiratory gas bladders for air breathing. By contrast, modern teleosts have developed respiratory organs in the head (buccal, pharyngeal, opercular) and along the digestive tract (esophagus, stomach, intestine) (Munshi, 1985; Silva et al., 1997; Satora and Winnicki, 2000; Podkowa and Goniakowska-Witalinska, 2002). The gills and gill derivatives, and the skin, also serve as ABOs in many species (Munshi, 1985; Graham, 1997; Graham et al., 2011; Maina, 2002a; Hsia et al., 2013). This work is focused on the structure of lungs and respiratory bladders. It aims to review basic morphological patterns and to highlight similarities and dissimilarities between lungs and gas bladders. The evolutionary aspects of these structures and the study of ABOs in more derived species are presented elsewhere in this issue. Neural and humoral control of ABO activity is also treated separately.