Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles

Abstract

The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (=Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a high-protein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field.

Inhibition of Local Immune Responses by the Frog-Killing Fungus Batrachochytrium dendrobatidis

“…A modified protocol in which PHA was injected intramuscularly into the feet of X. laevis was developed. The amount of swelling observed was between 3 and 20 times greater than previously recorded with subcutaneous injection in frogs (25)(26)(27)(28). The amount of inflammatory swelling induced by intramuscular injection was sufficient so that a noticeable difference was visible between PHA and buffer injections.…”

“…In birds, PHA is injected subcutaneously in avian patagia (wing-webs), and inflammation is measured by swelling at the site of injection (24). PHA induces robust T cell proliferation in vitro in amphibians (19,21) and can also induce in vivo inflammatory swelling in adults, metamorphs, and tadpoles (25)(26)(27)(28). In vivo, PHA induces swelling through the recruitment of granulocytes, phagocytes, thrombocytes, and lymphocytes (24,27).…”

Optimal digestion theory does not predict the effect of pathogens on intestinal plasticity

“…Opposite to the prediction from optimal digestion theory, when tadpoles are challenged with Bd, the relative lengths of their intestines decrease. Bd infections can reduce tadpole food consumption [7] and tadpoles that are resource limited have reduced defences against Bd [15]. Thus, one explanation for our results is that tadpoles divert energy resources from maintaining intestinal and overall growth towards deploying anti-parasite defences (e.g.…”

Exercise training reveals trade-offs among endurance performance and immune function, but not growth, in juvenile lizards

“…In adults, bacterial killing ability of plasma was significantly reduced by training, but there was no difference between the sexes (Husak et al, 2016). We did not have enough plasma to conduct such assays on juveniles, but because the complement immune system involved with bacterial killing is heavily dependent on protein availability (Venesky et al, 2012), we predict similar results. Future studies will reveal whether bacterial killing responds in the same way in juveniles as adults.…”