Morfofisiologia digestiva de Potamotrygon wallacei Carvalho, Rosa e Araujo (2016): uma espécie de arraia ornamental amazônica

Abstract

This study is a contribution to the digestive morphology and physiology of the freshwater stingray Potamotrygon wallacei, a neotropical elasmobranch species endemic to the Rio Negro basin (Central Amazon). Although popular as an ornamental fish, keeping this species in captivity often results in death from feeding problems and stress from confinement. The objective of the study was to investigate in detail the anatomy and physiology of the digestive tract (DT) of this stingray. As for the morphological aspects, techniques in conventional histology and tools in stereology were used to describe and quantify the different layers present in the stomach and spiral intestine. The functional aspects of DT were examined through the activities of the main digestive enzymes that act in proteolysis, lipolysis and hydrolysis of carbohydrates. To understand the interrelationships between the digestion of macronutrients (proteins, lipids and carbohydrates), a theoretical model was evaluated using Structural Equation Modeling (SEM). Morphologically, the esophagus has horizontal folds. The four histological layers are distinguishable: mucosa, submucosa, muscular (skeletal striated muscle) and serosa. The stratified mucosal epithelium has numerous PAS+ and Alcian blue+ mucosal cells, indicating secretion of neutral and acidic mucins, respectively. Residual activities of proteolytic, lipolytic and carbohydratease enzymes were found in the esophagus. However, these enzymes may represent endogenous intracellular activities, which suggests a limited role in the luminal digestion of ingested macronutrients. The stomach is U-shaped. The descending portion represents the cardiac region, while the ascending portion is the pyloric region. Regardless of the region, the histological layers of the stomach wall include: mucosa, submucosa, muscular (with inner and outer layers) and serosa. In the cardiac stomach, the mucous layer represents 44.7% of the total volume of the organ wall. Gastric glands (a component of the mucosa) occupy almost half the volume of the mucous layer. Proteolytic enzymes such as pepsin, trypsin, chymotrypsin and elastase, in addition to lipases, acid phosphatases, esterases and carbohydrateases are present. This indicates that the cardiac stomach has a high potential for digesting proteins, lipids and some carbohydrates. The density of gastric glands decreases and they become absent in the pyloric stomach. This explains a reduction in the capacity of digestive enzymes. However, the smooth muscle of the pyloric stomach wall becomes thicker due to the greater proportion of smooth muscle in the muscularis interna (circularis). Such a change suggests an active role of the pyloric stomach in the mixing process and aid in the passage of chyme to the spiral intestine. The spiral gut (spiral valve) has 10-11 loops histologically made up of simple columnar epithelium, lamina propria (loose connective tissue), and scattered smooth muscle. The epithelium is almost exclusively formed by absorptive cells (enterocytes) and rare mucous cells. The lamina propria has numerous blood vessels. The wall of the spiral valve has four tissue layers: mucosa, submucosa, muscularis, and serosa. The density of epithelial tissue tends to decrease, while the proportion of submucosa increases. This indicates a trend in the ability to transport nutrients into blood vessels. The spiral intestine is the final seat of digestion of proteins, lipids and carbohydrates. The high activities of endopeptidases (trypsin, chymotrypsin and elastase), as well as exopeptidase, leucine aminopeptidase, reinforce the proteolytic potential of the spiral valve in protein digestion. Lipolytic capacity and carbohydrate hydrolysis are also high at this site. SEM-based models suggest strong dependence between these three catabolic pathways in different organs of the digestive tract. Finally, the morphological and digestive enzyme data are consistent with the information on the diet of P. wallacei, a carnivorous stingray that consumes mainly crustaceans, insect larvae and small fish. The results of this study can contribute to the development of good management practices in the feeding of stingrays in captivity, aiming at the preservation of the species and the well-being of individuals in confined environments.