Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

Abstract

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

Morphofunctional description of mucous cells in the gills of the Arapaimidae Arapaima gigas (Cuvier) during its development

“…A morphological analysis of the gill epithelium of A. gigas describing the presence of PCs with short microridges has been performed by Ramos et al. (). According to Kendall and Dale (), the function of microridges may be to increase the epithelial surface area where gas exchange occurs and to create a slower flow of water over cells to optimize gas exchange.…”

“…In addition, several studies (Gonzalez, Wilson, & Wood, ; Matsuo & Val, ; Steinberg et al., ; Wood et al., ) report that humic substances dissolved in blackwater contribute to the prevention of ion loss. Considering the type of habitat in which A. gigas is found, its epithelial thickening may increase in the activity of CCs in these animals (Ramos et al., ). The hypothesis that mucus secreted by MCs plays a role in ion attraction to favour ion exchange is acceptable.…”

“…Therefore, there are two hypotheses that may explain this finding. The first one is that A. gigas gill remodelling (embedding lamellae in filament tissue) ensures that in animals over ≈500 g, the lamellae epithelial thickness is increased (Ramos et al., ). In this sense, we suppose that gill remodelling does not result in significant changes in the osmorespiratory compromise because A. gigas obtains O 2 by breathing air, which means that gills are more protected against bacterial and parasitic infections due to increased MC secretion, as shown in the present study.…”

“…In contrast, in adult A. gigas, the gills are not able to obtain enough O 2 to meet the animal's physiological needs, and O 2 absorption occurs mainly through the modified swim bladder. Thus, there is a change in gill function so that from the fry stage to the adult stage, following remodelling of the gill epithelium, gills become mainly involved in ion regulation (Gonzalez et al., ; Ramos, ; Ramos, Fernandes, Costa, & Duncan, ).…”

Hematological adjustments of the bony tongue Arapaima gigas under influence of amazonian waters

“…Despite being an air breather its gill structure is quite close to water breathers, especially in early stages of development [1]. However, in animals above 100g the pillar cell system are embedded into the filament being the gill, an ion regulation active site.…”