Chemical composition of food induces plasticity in digestive morphology in larvae of Rana temporaria

Abstract

Food conditions are changing due to anthropogenic activities and natural sources and thus, many species are exposed to new challenges. Animals might cope with altered quantitative and qualitative composition [i.e. variable protein, nitrogen (N) and energy content] of food by exhibiting trophic and digestive plasticity. We examined experimentally whether tadpoles of the common frog (Rana temporaria) exhibit phenotypic plasticity of the oral apparatus and intestinal morphology when raised on a diet of either low (i.e. Spirulina algae) or high protein, N and energy content (i.e. Daphnia pulex). Whereas intestinal morphology was highly plastic, oral morphology did not respond plastically to different chemical compositions of food. Tadpoles that were fed food with low protein and N content and low-energy density developed significantly longer guts and a larger larval stomachs than tadpoles raised on high protein, N and an energetically dense diet, and developed a different intestinal surface morphology. Body sizes of the treatment groups were similar, indicating that tadpoles fully compensated for low protein, N and energy diet by developing longer intestines. The ability of a species, R. temporaria, to respond plastically to environmental variation indicates that this species might have the potential to cope with new conditions during climate change.

Keywords: Adaptability; Climate change; Gut length; Nutrient content; Oral papillae; Protein content.

Fig. 1.

Body sizes of R. temporaria tadpoles under low protein, N and energy content (Spirulina) and high protein, N and energy content food conditions (Daphnia). Shown are medians, 25% and 75% percentiles (boxes) and minimum and maximum values (whiskers). No statistical difference between the two treatments.

Fig. 2.

Relative gut length. Residuals of gut length versus body length of R. temporaria tadpoles under low protein, N and energy content (Spirulina) and high protein, N and energy content food conditions (Daphnia). Shown are medians, 25% and 75% percentiles (boxes) and minimum and maximum values (whiskers). The guts of Spirulina-fed tadpoles were significantly longer than those of Daphnia-fed tadpoles (U-test: n=14, P<0.001).

Fig. 3.

Relative volume of the larval stomach Manicotto glandulare. Residuals of Manicotto glandulare volume versus body length of R. temporaria tadpoles under low protein, N and energy content (Spirulina) and high protein, N and energy content food conditions (Daphnia). Shown are medians, 25% and 75% percentiles (boxes) and minimum and maximum values (whiskers). The Manicotto of Spirulina-fed tadpoles were significantly larger than of Daphnia-fed tadpoles (U-test: n=14, P<0.04).

Fig. 4.

Intestinal microstrcutures (microvilli seam) of larval R. temporaria. Intestinal microstructures (microvilli seam) of R. temporaria tadpoles under high protein, N and energy content (Daphnia; A,C) and low protein, N and energy content food conditions (Spirulina; B,D). Shown are pictures taken by electron microscopy at 2600× (A,B) and 47,000× magnification (C,D).