Carry-Over Effects of Desiccation Stress on the Oxidative Status of Fasting Anuran Juveniles

Abstract

Amphibians are sensitive to deteriorating environmental conditions, especially during transition to a terrestrial environment which is full of uncertainties. Harsh conditions, such as desiccation during earlier stages, affect different larval traits with possible carry-over effects on juvenile and adult life histories. The first consequences of the effects can be seen in juveniles in the challenges to find food and the ability to survive without it in a terrestrial habitat. Body size and the internal energy reserves acquired during the larval phase play an important role in this period. Herein, we tested how different water regimes (low water availability, desiccation and constant high-water availability) during larval development reflect on the oxidative status and ability of yellow belly toad (Bombina variegata) juveniles to endure short-term fasting. The desiccation regime significantly reduced the body size of metamorphs. The same was observed after 2 weeks of fasting, while the feeding treatment reduced differences mostly in the body mass of individuals from different water regimes. This was the result of a greater gain in mass in juveniles pre-exposed to desiccation. Pre-exposure to desiccation also modified the parameters of the antioxidant system (AOS) under feeding conditions, leading to higher values of superoxide dismutase, glutathione reductase and glutathione S-transferase, glutathione and sulfhydryl group concentrations, and lower glutathione peroxidase in comparison to juveniles reared under constant water. The increase in the AOS of juveniles can be considered as a physiological carry-over effect of desiccation, probably as the result of compensatory growth and/or earlier exposure to chronic stress. However, water levels during larval development did not exert significant effects on the oxidative status of juveniles subjected to food unavailability. Fasting juveniles, both control and desiccated, were exposed to oxidative stress, significantly higher lipid peroxide concentrations, lower superoxide dismutase, glutathione peroxidase, glutathione S-transferase, glutathione and sulfhydryl group values in comparison to feeding individuals. The lack of food in juvenile anurans activated the AOS response in the same manner, regardless of body size and stress pre-exposure, suggesting that the generally accepted hypothesis about the influence of metamorphic body size on the fitness of the postmetamorphic stage should be tested further.

Keywords: Bombina variegate; amphibians; antioxidant system; development; food deprivation; oxidative stress; pond drying; yellow belly toad.

FIGURE 1

Biometric parameters: snout-vent length [(A)– SVL in mm], body mass [(B)– BM in g] and body condition index [(C)– BCI] at the start and end of the fasting/feeding treatment for individual that developed under conditions of desiccation and constant water. CC, feeding individuals that developed under constant water availability; CF, fasting individuals that developed under constant water availability; DC, feeding individuals that developed under exposure to the desiccation regime; DF, fasting individuals that developed under the desiccation regime. SVL and BM are given as mean ± standard error of raw data, BCI on log-transformed data. “#” indicates significant differences between same groups at the end and start of treatment; “*” indicates significant differences between fasting and feeding treatments under the same water regime; capital letters “A” and “B” indicate differences between feeding individuals exposed to desiccation and constant water availability (start vs. start, and end vs. end); lower case letters “a” and “b” indicate differences between fasting individuals exposed to desiccation and constant water (start vs. start, and end vs. end). Different letters indicate significant differences (P ≤ 0.05). Line, Mean value; box, Standard error; bars, Minimal and maximal value.

FIGURE 2

Effects of 2-weeks of fasting/feeding treatment on oxidative stress parameters of the yellow belly toad (Bombina variegata) juveniles that developed under constant and decreasing water levels. CC, Feeding individuals that developed under constant water availability; CF, Fasting individuals that developed under constant water availability; DC, Feeding individuals that developed under exposure to the desiccation regime; DF, Fasting individuals that developed under the desiccation regime. (A) Catalase; (B) superoxide dismutase; (C) glutathione peroxidase; (D) lipid peroxidation; (E) glutathione; (F) glutathione reductase; (G) glutathione-S transferase; (H) SH groups. “*” indicates significant differences between fasting and feeding treatments under the same water regime; capital letters “A” and “B” indicate differences between feeding individuals exposed to desiccation and constant water availability; lower case letters “a” and “b” indicate differences between fasting individuals exposed to desiccation and constant water. Different letters indicate significant differences (P ≤ 0.05). Line, Mean value; box, Standard error; bars, Minimal and maximal value.