Effects of the nematodeGyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism

Abstract

We describe a novel mutualism between bullfrog tadpoles (Rana catesbeiana) and a tadpole-specific gastrointestinal nematode (Gyrinicola batrachiensis). Groups of tadpoles were inoculated with viable or nonviable nematode eggs, and development, morphology, and gut fermentation activity were compared between nematode-infected and uninfected tadpoles. Nematode infection accelerated tadpole development; the mean time to metamorphosis was 16 d shorter and the range of times to metamorphosis was narrower in nematode-infected tadpoles than in uninfected tadpoles. At metamorphosis, infected and uninfected bullfrogs did not differ in body size or condition. Colon width, wet mass of colon contents, and concentrations of most fermentation byproducts (short-chain fatty acids: SCFAs) in the hindgut were greater in infected tadpoles. Furthermore, in vitro fermentation yields for all SCFAs combined were over twice as high in infected tadpoles than in uninfected tadpoles. One explanation for accelerated development in infected tadpoles is the altered hindgut fermentation associated with the nematodes. Energetic contributions of fermentation were estimated to be 20% and 9% of the total daily energy requirement for infected and uninfected tadpoles, respectively. Infection by G. batrachiensis nematodes potentially confers major ecological and evolutionary advantages to R. catesbeiana tadpoles. The mutualism between these species broadens our understanding of the taxonomic diversity and physiological contributions of fermentative gut symbionts and suggests that nematodes inhabiting the gut regions of other ectothermic herbivores might have beneficial effects in those hosts.

Revisiting “what do tadpoles really eat?” A 10‐year perspective

“…Schiesari et al (2009) used stable isotope analysis to examine the trophic ecology of four ranid species (Lithobates catesbeianus, Lithobates clamitans, Lithobates sylvaticus, and Lithobates pipiens) coexisting in six natural wetlands in Michigan. These results contradicted previous studies suggesting that L. catesbeianus and L. sylvaticus tadpoles are primarily herbivorous and omnivorous, respectively (Petranka, Hopey, Jennings, Baird, & Boone, 1994;Pryor & Bjorndal, 2005), and highlighted that tadpoles can exhibit great degree of diet variation, both spatially and temporally. These results contradicted previous studies suggesting that L. catesbeianus and L. sylvaticus tadpoles are primarily herbivorous and omnivorous, respectively (Petranka, Hopey, Jennings, Baird, & Boone, 1994;Pryor & Bjorndal, 2005), and highlighted that tadpoles can exhibit great degree of diet variation, both spatially and temporally.…”

“…In particular, metagenomics (i.e. Early studies based on gut analysis (Bjorndal, 1997;Pryor, 2008;Pryor & Bjorndal, 2005) suggested that the digestive tracts of tadpoles contained a high diversity of microorganisms, including anaerobic and aerobic bacteria, ciliates, and nematodes. Metagenomic data using 16S rRNA gene sequencing provide genetic information on the entire gut microbiome, allowing for the characterisation of gut community structure and composition (Garmendia, Hernandez, Sanchez, & Martinez, 2012).…”

Comparison of intestinal microbes in female and male Chinese concave‐eared frogs (Odorrana tormota) and effect of nematode infection on gut bacterial communities

“…However, Lukeš, Stensvold, Jirků‐Pomajbíková, and Wegener Parfrey () promoted the idea of some parasites being beneficial to the host rather than culprits of disease. For example, a mutualistic relationship exists between bullfrog tadpoles ( Rana catesbeiana ) and a tadpole‐specific gastrointestinal nematode ( Gyrinicola batrachiensis ; Pryor & Bjorndal, ). As yet, the complex interactions between helminths, gut microbiota, and the host have not been adequately studied in wild species (Kreisinger, Bastien, Hauffe, Marchesi, & Perkins, ).…”

Microbiota and Mucosal Immunity in Amphibians

“…Several small chain fatty acids such as acetate, butyrate, and propionate are produced by fermentation in the small intestine and in the colon (117). The microbiodiversity of the gut in these tadpoles is complex since it includes not only bacteria but also ciliated protozoans, parasites, and some symbiotic nematodes (120). …”