Long‐term starvation in cave salamander effects on liver ultrastructure and energy reserve mobilization

Abstract

The morphological alterations of hepatocytes of cave-dwelling salamander Proteus anguinus anguinus after food deprivation periods of one and 18 months were investigated and the concentrations of glycogen, lipids, and proteins in the liver were determined. Quantitative analyses of the hepatocyte size, the lipid droplets, the number of mitochondria, and volume densities of M and P in the hepatocytes were completed. After one month of food deprivation, the cytological changes in the hepatocytes are mainly related to the distribution and amount of glycogen, which was dispersed in the cytoplasm and failed to form clumps typical of normal liver tissue. After 18 months of food deprivation hepatocytes were reduced in size, lipid droplets were less numerous, peroxisomes formed clusters with small, spherical mitochondria, and specific mitochondria increased in size and lost cristae. Lysosomes, autophagic vacuoles, and clear vacuoles were numerous. The liver integrity was apparently maintained, no significant loss of cytoplasmic constituents have been observed. Biochemical analysis revealed the utilization of stored metabolic reserves in the liver during food deprivation. Glycogen is rapidly utilized at the beginning of the starvation period, whereas lipids and proteins are utilized subsequently, during prolonged food deprivation. In the Proteus liver carbohydrates are maintained in appreciable amounts and this constitutes a very important energy depot, invaluable in the subterranean environment.

Molecules, Mechanisms, and Disorders of Self-Domestication: Keys for Understanding Emotional and Social Communication from an Evolutionary Perspective

“…Obligatory neoteny is also seen in the olm (Proteus anguinus), which, in addition to its weight (only 15-20 g), resembles axolotls in many aspects (e.g., it has external gills and small legs). The olm is well adapted to long-term starvation [53], reaches sexual maturity at about 15.6 years of age, and lays about 35 eggs every 12.5 years. The average recorded life expectancy in captivity is 68.5 years, while the maximum life expectancy is estimated at 103 years [54].…”

Differential Proteomic Analysis of Chinese Giant Salamander Liver in Response to Fasting

“…The liver is the central organ for metabolic activity in vertebrates and is also an important storage depot for energy reserve (glycogen and lipids). Urodele amphibians not only have large amounts of glycogen in hepatocytes, but also have larger amount of lipids than other vertebrates (Bizjak Mali et al, 2013). Hepatic fat serves as energy reserve in many vertebrates including fishes and amphibians during starvation (Groom et al, 2013).…”

“…The utilization of the energy reserves varies in different species with successive periods of glycogen, lipid, and finally lipid-protein-dominant catabolism. For hypogean salamander Proteus anguinus that can tolerate fasting for between 18 and 96 months, its liver glycogen was decreased by 50%, lipids by 25%, and proteins by 35% after 18 months of starvation (Hervant et al, 2001;Bizjak Mali et al, 2013). Reduced hepatocyte size, scarce lipid droplets, and numerous mitochondria and peroxisomes were observed in the hepatocytes of P. anguinus after 18 months of starvation (Bizjak Mali et al, 2013).…”

“…For hypogean salamander Proteus anguinus that can tolerate fasting for between 18 and 96 months, its liver glycogen was decreased by 50%, lipids by 25%, and proteins by 35% after 18 months of starvation (Hervant et al, 2001;Bizjak Mali et al, 2013). Reduced hepatocyte size, scarce lipid droplets, and numerous mitochondria and peroxisomes were observed in the hepatocytes of P. anguinus after 18 months of starvation (Bizjak Mali et al, 2013). For the frog Rana esculenta, its liver glycogen concentration decreased by 95% after 18 months of starvation at 20 • C (Grably and Piery, 1981).…”

First microsatellite data on Proteus anguinus reveal weak genetic structure between the caves of Postojna and Planina

“…Although formal protection of proteus and its habitat is high at both national and European levels, its true conservation status is poorly known and regionally unfavourable (Bressi, ; Hudoklin, ). As an enigmatic, paedomorphic animal it has attracted research by many disciplines, including developmental biology (Sessions, Bulog, & Bizjak Mali, ), longevity (Voituron, de Fraipont, Issartel, Guillaume, & Clobert, ), sex chromosome evolution (Sessions, Bizjak Mali, Green, Trifonov, & Ferguson‐Smith, ) and starvation (Bizjak Mali, Sepčić, & Bulog, ).…”