In light of the relationship of lungfish to the origin of tetrapods, information on the respiratory biology of lungfish can give insight into the functional morphological and physiological prerequisites for the conquest of land by the first tetrapods. Stereological methods were employed in order to determine the respiratory surface area and thickness of the water-blood barrier or air-blood of the gills, lungs, and skin, respectively, of the South American lungfish Lepidosiren paradoxa. The morphometric diffusing capacity was then determined by multiplying by the appropriate Krogh diffusion constants (K). Our results indicate a total diffusing capacity of all respiratory organs of 0.11 mL min(-1) mmHg(-1) kg(-1), which is more than twice the value of the physiological diffusion capacity (approximately 0.04 mL min(-1) mmHg(-1) kg(-1)). Of this, 99.15% lies in the lungs, 0.85% in the skin, and only 0.0013% in the gills. Since K for CO(2) is 20-25 times greater than for O(2), diffusing capacity of CO(2) through the skin is potentially important. That of the gills, however, is negligible, raising the question as to their function. Our results indicate that the morphological prerequisites for terrestrial survival with regard to supporting aerobic metabolism already existed in the lungfish.
SummaryPrevious morphometric methods for estimation of the volume of components, surface area and thickness of the diffusion barrier in fish gills have taken advantage of the highly ordered structure of these organs for sampling and surface area estimations, whereas the thickness of the diffusion barrier has been measured orthogonally on perpendicularly sectioned material at subjectively selected sites. Although intuitively logical, these procedures do not have a demonstrated mathematical basis, do not involve random sampling and measurement techniques, and are not applicable to the gills of all fish. The present stereological methods apply the principles of surface area estimation in vertical uniform random sections to the gills of the Brazilian teleost Arapaima gigas. The tissue was taken from the entire gill apparatus of the right-hand or left-hand side (selected at random) of the fish by systematic random sampling and embedded in glycol methacrylate for light microscopy. Arches from the other side were embedded in Epoxy resin. Reference volume was estimated by the Cavalieri method in the same vertical sections that were used for surface density and volume density measurements. The harmonic mean barrier thickness of the water-blood diffusion barrier was calculated from measurements taken along randomly selected orientation lines that were sine-weighted relative to the vertical axis. The values thus obtained for the anatomical diffusion factor (surface area divided by barrier thickness) compare favourably with those obtained for other sluggish fish using existing methods.
The gill structure of the Amazonian fish Arapaima gigas, an obligatory air breather, was investigated during its transition from water breathing to the obligatory air breathing modes of respiration. The gill structure of A. gigas larvae is similar to that of most teleost fish; however, the morphology of the gills changes as the fish grow. The main morphological changes in the gill structure of a growing fish include the following: (1) intense cell proliferation in the filaments and lamellae, resulting in increasing epithelial thickness and decreasing interlamellar distance; (2) pillar cell system atrophy, which reduces the blood circulation through the lamellae; (3) the generation of long cytoplasmic processes from the epithelial cells into the intercellular space, resulting in continuous and sinuous paracellular channels between the epithelial cells of the filament and lamella that may be involved in gas, ion, and nutrient transport to epithelial cells; and (4) intense mitochondria-rich cell (MRC) proliferation in the lamellar epithelium. All of these morphological changes in the gills contribute to a low increase of the respiratory surface area for gas exchange and an increase in the water-blood diffusion distance increasing their dependence on air-breathing as fish developed. The increased proliferation of MRCs may contribute to increased ion uptake, which favors the regulation of ion content and pH equilibrium. Anat Rec, 296:1664Rec, 296: -1675
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.