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

Abstract

One prediction of optimal digestion theory is that organisms will increase the relative length of their digestive tracts when food resources become limited. We used theory of optimal digestion to test whether tadpoles can adjust the relative length of their intestines when challenged with the fungal pathogen Batrachochytrium dendrobatidis (Bd). The degree of tadpole mouthpart damage, a symptom of Bd infections that reduces food consumption, was associated positively with the length of tadpole intestines relative to their body size, consistent with optimal digestion theory. After controlling for mouthpart damage, tadpoles exposed to Bd had shorter intestines relative to their body size, opposite to the predictions of optimal digestion theory. One explanation of why tadpoles with higher Bd loads have shorter relative intestinal lengths is that they divert energy from maintaining intestinal and overall growth towards anti-parasite defences.

Batrachochytrium dendrobatidis exposure effects on foraging efficiencies and body size in anuran tadpoles

“…In our experiment, significant mouthpart damage was observed in both Bd exposed and unexposed subjects, a results that has been observed previously (Venesky et al 2013). Because the loose food that was added to the containers often sank, tadpoles were forced to scour the bottoms of the containers, likely contributing to mouthpart damage in both treatments.…”

“…Two specific paths were observed in the Bd exposure group, one from Bd to gut content to body size, and one from mouthpart damage to gut content to body size. Counter to our hypothesis, Bd exposure did not affect body size through the Bd to mouthpart damage to gut content to body size pathway, likely due to high mouthpart damage in both Bd-exposed and unexposed treatments.In our experiment, significant mouthpart damage was observed in both Bd exposed and unexposed subjects, a results that has been observed previously (Venesky et al 2013). Because the loose food that was added to the containers often sank, tadpoles were forced to scour the bottoms of the containers, likely contributing to mouthpart damage in both treatments.…”

“…While previous studies have shown relationships between Bd exposure and mouthpart damage (Venesky et al 2013), amount of food ingested (Venesky et al 2010), and growth (Parris & Cornelius 2004), our study shows the interrelatedness of these responses. Two specific paths were observed in the Bd exposure group, one from Bd to gut content to body size, and one from mouthpart damage to gut content to body size.…”

“…While non-lethal, Bd-induced damage to tadpole mouthparts has been shown to reduce foraging efficiencies (Venesky et al 2009) and reduce tadpole growth (Venesky et al 2009(Venesky et al , 2013; but see Hanlon et al 2012, Kleinhenz et al 2012. Recently, Venesky et al (2013) showed that Bd exposure reduced tadpole size, and mouthpart damage reduced the size of tadpole guts relative to body size. In other words, studies have shown that Bd causes mouthpart damage, damage reduces foraging efficiency, and reduced efficiency reduces growth.…”

“…As keratin occurs in the mouthparts of tadpoles in most species (McDiarmid & Altig 1999), Bd also infects tadpole mouthparts; however it is not usually a direct cause of mortality (but see Searle et al 2013, Hanlon & Parris 2014. While non-lethal, Bd-induced damage to tadpole mouthparts has been shown to reduce foraging efficiencies (Venesky et al 2009) and reduce tadpole growth (Venesky et al 2009(Venesky et al , 2013; but see Hanlon et al 2012, Kleinhenz et al 2012. Recently, Venesky et al (2013) showed that Bd exposure reduced tadpole size, and mouthpart damage reduced the size of tadpole guts relative to body size.…”