Gut bacterial communities across tadpole ecomorphs in two diverse tropical anuran faunas
- 856 Downloads
Animal-associated microbial communities can play major roles in the physiology, development, ecology, and evolution of their hosts, but the study of their diversity has yet focused on a limited number of host species. In this study, we used high-throughput sequencing of partial sequences of the bacterial 16S rRNA gene to assess the diversity of the gut-inhabiting bacterial communities of 212 specimens of tropical anuran amphibians from Brazil and Madagascar. The core gut-associated bacterial communities among tadpoles from two different continents strongly overlapped, with eight highly represented operational taxonomic units (OTUs) in common. In contrast, the core communities of adults and tadpoles from Brazil were less similar with only one shared OTU. This suggests a community turnover at metamorphosis. Bacterial diversity was higher in tadpoles compared to adults. Distinct differences in composition and diversity occurred among gut bacterial communities of conspecific tadpoles from different water bodies and after experimental fasting for 8 days, demonstrating the influence of both environmental factors and food on the community structure. Communities from syntopic tadpoles clustered by host species both in Madagascar and Brazil, and the Malagasy tadpoles also had species-specific isotope signatures. We recommend future studies to analyze the turnover of anuran gut bacterial communities at metamorphosis, compare the tadpole core communities with those of other aquatic organisms, and assess the possible function of the gut microbiota as a reservoir for protective bacteria on the amphibian skin.
KeywordsAmphibia Anura Tadpoles Gut microbiota 16S rRNA Stable isotopes
Work in Madagascar was made possible by a collaboration accord between the Université d’Antananarivo (Département de Biologie Animale), the Ministère de l’Environnement, des Eaux et Forêts of the Republic of Madagascar, and the Technische Universität Braunschweig. We are grateful to the Malagasy authorities for research and export permits. We are deeply indebted to Otto Larink (TU Braunschweig) for his kind help with identifying the tadpole food items. Meike Kondermann was of invaluable help with lab work. Work in Madagascar was supported by the Volkswagen Foundation to MV, JG, and RDR; by grants of the Deutsche Forschungsgemeinschaft to MV (VE247/2-1 and VE247/9-1) and JG (GL 665/1-1); and by fellowships of the Deutscher Akademischer Austauschdienst to MB and RDR. Maria J. O. Campos and Marcelo de Carvalho authorized our entry into the work area in Itapé, Rio Claro, SP, Brazil. Work in Brazil was supported by a visiting researcher grant of CAPES to MV, CFBH, and ML (88881.062205/2014-01). CFBH thanks grant #2013/50741-7, São Paulo Research Foundation (FAPESP) and CNPq, for a research fellowship. Experiments were approved by the Ethics Committee of UNESP Rio Claro (permit no. 36/2015).
- Altig R, McDiarmid RW (1999) Body plan: development and morphology. In: McDiarmid RW, Altig R (eds) Tadpoles. The biology of anuran larvae. The University of Chicago Press, Chicago, pp 24–51Google Scholar
- Aronesty E (2011) ea–utils: Command–line tools for processing biological sequencing data. http://code.google.com/p/ea–utils. Accessed 1 Oct 2015
- Bjorndal KA, Pryor GS (2005) Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism. J Exp Zool Part A 303:704–712Google Scholar
- Grosjean S, Randrianiaina R-D, Strauß A, Vences M (2011b) Sand-eating tadpoles in Madagascar: morphology and ecology of the unique larvae of the treefrog Boophis picturatus. Salamandra 47:63–76Google Scholar
- Inger RF (1986) Diets of tadpoles living in a Borneo rain forest. Alytes 5:153–164Google Scholar
- Oliveros JC (2015) Venny. An interactive tool for comparing lists with Venn’s diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html. Accessed 1 Oct 2015
- Pryor GS (2008) Anaerobic bacteria isolated from the gastrointestinal tracts of bullfrog tadpoles (Rana catesbeiana). Herpetol Conserv Biol 3:176–181Google Scholar
- Schmidt H, Strauß A, Reeve E, Letz A, Ludewig AK, Neb D, Pluschzick R, Randrianiaina RD, Reckwell D, Schröder S, Wesolowski A, Vences M (2008) Descriptions of the remarkable tadpoles of three treefrog species, genus Boophis, from Madagascar. Herpetol Notes 1:49–57Google Scholar
- Strauß A, Reeve E, Randrianiaina RD, Vences M, Glos J (2010) The world’s richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar’s stream-dwelling amphibian larvae. BMC Ecol 10:12. doi: 10.1186/1472-6785-10-12 CrossRefPubMedPubMedCentralGoogle Scholar
- Viertel B, Richter S (1999) Anatomy: viscera and endocrines. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, pp 92–148Google Scholar
- Zina J, Ennser J, Pinheiro SCP, Haddad CFB, Toledo LF (2007) Taxocenose de anuros de uma mata semidecídua do interior do Estado de São Paulo e comparações com outras taxocenoses do Estado, sudeste do Brasil. Biota Neotropical 7:1–9Google Scholar