Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard

Abstract

While herbivory is a common feeding strategy in a number of vertebrate classes, less than 4% of squamate reptiles feed primarily on plant material. It has been hypothesized that physiological or microbial limitations may constrain the evolution of herbivory in lizards. Herbivorous lizards exhibit adaptations in digestive morphology and function that allow them to better assimilate plant material. However, it is unknown whether these traits are fixed or perhaps phenotypically flexible as a result of diet. Here, we maintained a naturally omnivorous lizard, Liolaemus ruibali, on a mixed diet of 50% insects and 50% plant material, or a plant-rich diet of 90% plant material. We compared parameters of digestive performance, gut morphology and function, and gut microbial community structure between the two groups. We found that lizards fed the plant-rich diet maintained nitrogen balance and exhibited low minimum nitrogen requirements. Additionally, lizards fed the plantrich diet exhibited significantly longer small intestines and larger hindguts, demonstrating that gut morphology is phenotypically flexible. Lizards fed the plant-rich diet harbored small intestinal communities that were more diverse and enriched in Melainabacteria and Oscillospira compared with mixed diet-fed lizards. Additionally, the relative abundance of sulfate-reducing bacteria in the small intestine significantly correlated with whole-animal fiber digestibility. Thus, we suggest that physiological and microbial limitations do not sensu stricto constrain the evolution of herbivory in lizards. Rather, ecological context and fitness consequences may be more important in driving the evolution of this feeding strategy.

Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission

“…A controlled feeding trial using L. ruibali demonstrated that the abundance of Desulfovibrio in the small intestine was correlated with whole‐animal fibre digestibility (Kohl et al . ). Further, the presence of Desulfovibrio may be important for reducing the H 2 by‐products associated with anaerobic fermentation in herbivorous iguanas (Hong et al .…”

“…Further details for housing and feeding of L. parvus and L. ruibali can be found in Kohl et al . (). We fed Phymaturus williamsi in the same manner as described in Kohl et al .…”

“…We fed Phymaturus williamsi in the same manner as described in Kohl et al . (), but used a diet of ground rabbit chow mixed with water (approximately 30% rabbit chow: 70% water) and an amount of ~9.8 mg dry food/gram body mass every other day.…”

“…Lizards were kept in small plastic cages with autoclaved soil and given access to autoclaved water ad libitum. Further details for housing and feeding of L. parvus and L. ruibali can be found in Kohl et al (2016). We fed Phymaturus williamsi in the same manner as described in Kohl et al (2016), but used a diet of ground rabbit chow mixed with water (approximately 30% rabbit chow: 70% water) and an amount of~9.8 mg dry food/gram body mass every other day.…”

Microbial communities exhibit host species distinguishability and phylosymbiosis along the length of the gastrointestinal tract

“…For example, ruminants fed fresh forage exhibit higher abundances of Oscillospira compared to those fed low‐fibre grain, and microscopy reveals that these bacteria associate with the surfaces of plant material in the gut (Mackie et al., ). Further, high‐fibre diets increase the abundance of Oscillospira in the guts of lizards (Kohl et al., ). The rodents in our study may maintain higher abundance of Ruminococcus and Oscillospira in the hindgut to aid in the digestion of dietary fibre.…”