Journal Home > Volume 13 , Issue 3
Avian Research 2022, 13(3): 100050 https://doi.org/10.1016/j.avrs.2022.100050
Research Article | Open Access | Issue | Published: 19 July 2022

Comparative analysis of the intestinal tract microbiota and feeding habits of five sympatric flycatchers

Show Author's Information Zhehan Donga,  Shangmingyu Zhanga,  Yuwen Chenga,  Xingcheng Hea,  Ian Haasea,  Yi Liangb,  Yong Jiangc,  Yongjie Wua( )
Key Laboratory of Bio-Resources and Eco-Environment, Ministry of Education, College of Life Science, Sichuan University, Chengdu, 610065, China
The General Work Station of Protected Area of Sichuan Province, Sichuan Forestry and Grassland Bureau, Chengdu, 610081, China
Administration of Gongga Mountain National Nature Reserve, Kangding, Ganzi Tibetan Autonomous Prefecture, 626000, China
Keywords:
Gut microbiota, Sympatric, Feeding habit, Gastrointestinal tract, Insectivorous, Muscicapidae
Cite this article:
Dong Z, Zhang S, Cheng Y, et al. Comparative analysis of the intestinal tract microbiota and feeding habits of five sympatric flycatchers. Avian Research, 2022, 13(3): 100050. https://doi.org/10.1016/j.avrs.2022.100050
Download citation
EndNote(RIS)
BibTeX

468

Views

16

Downloads

Citations

1

Crossref

1

WoS

1

Scopus

0

CSCD

Abstract Full text About this article

Gut microbiota and host interactions co-evolve and develop into stably adapted microbial communities and play vital roles in maintaining the health of organisms. Diet is supposed to be an important driver of differences in gut microbiota, but previous studies would commonly use literature depictions, which are essential but inaccurate, to explain the effects of diet on the gut microbiota of wild birds. In this study, we collected intestinal samples from five sympatric flycatchers to compare the gut microbial differences using bacterial 16S rRNA genes from Illumina MiSeq platform. Over 1,642,482 quality-filtered sequences from 18 16S rRNA libraries were obtained and distinct compositions and diversities of gut microbiota were found in five flycatchers. Their gut microbiota is mainly from the four bacterial phyla of Proteobacteria, Firmicutes, Actinomycetes, and Bacteroidetes, but at the genus level showed a significant difference. Functional predictions revealed that the metabolic capacity of the gut microbiota of five flycatchers is greatly distinguished at KEGG level 3. And multiple food fragments showed a significant correlation with gut microbiota. Besides, the significant differences in the specific composition of the diets of the five insectivorous flycatchers indicated the differentiation of dietary niches. The study of the gut microbiota and feeding habits of sympatric flycatchers would increase the understanding of the gut microbial diversity of wild birds, and also improve our cognition of the co-evolution and co-adaptation within the host gut microbiota relations.


menu
Abstract
Full text
Outline
About this article

Comparative analysis of the intestinal tract microbiota and feeding habits of five sympatric flycatchers

Show Author's information Zhehan Donga, Shangmingyu Zhanga, Yuwen Chenga, Xingcheng Hea, Ian Haasea, Yi Liangb, Yong Jiangc, Yongjie Wua( )
Key Laboratory of Bio-Resources and Eco-Environment, Ministry of Education, College of Life Science, Sichuan University, Chengdu, 610065, China
The General Work Station of Protected Area of Sichuan Province, Sichuan Forestry and Grassland Bureau, Chengdu, 610081, China
Administration of Gongga Mountain National Nature Reserve, Kangding, Ganzi Tibetan Autonomous Prefecture, 626000, China

Abstract

Gut microbiota and host interactions co-evolve and develop into stably adapted microbial communities and play vital roles in maintaining the health of organisms. Diet is supposed to be an important driver of differences in gut microbiota, but previous studies would commonly use literature depictions, which are essential but inaccurate, to explain the effects of diet on the gut microbiota of wild birds. In this study, we collected intestinal samples from five sympatric flycatchers to compare the gut microbial differences using bacterial 16S rRNA genes from Illumina MiSeq platform. Over 1,642,482 quality-filtered sequences from 18 16S rRNA libraries were obtained and distinct compositions and diversities of gut microbiota were found in five flycatchers. Their gut microbiota is mainly from the four bacterial phyla of Proteobacteria, Firmicutes, Actinomycetes, and Bacteroidetes, but at the genus level showed a significant difference. Functional predictions revealed that the metabolic capacity of the gut microbiota of five flycatchers is greatly distinguished at KEGG level 3. And multiple food fragments showed a significant correlation with gut microbiota. Besides, the significant differences in the specific composition of the diets of the five insectivorous flycatchers indicated the differentiation of dietary niches. The study of the gut microbiota and feeding habits of sympatric flycatchers would increase the understanding of the gut microbial diversity of wild birds, and also improve our cognition of the co-evolution and co-adaptation within the host gut microbiota relations.

Keywords: Gut microbiota, Sympatric, Feeding habit, Gastrointestinal tract, Insectivorous, Muscicapidae

References(68)

Al-Asmakh, M., Stukenborg, J.B., Reda, A., Anuar, F., Strand, M.L., Hedin, L., et al., 2014. The gut microbiota and developmental programming of the testis in mice. PLoS One 9, e103809.
DOI Google Scholar

Amato, K.R., Sanders, J.G., Song, S.J., Nute, M., Metcalf, J.L., Thompson, L.R., et al., 2019. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576-587.
DOI Google Scholar

Barçante, L., Vale, M.M., Maria, M.A., 2017. Altitudinal migration by birds: a review of the literature and a comprehensive list of species. J. Field Ornithol. 88, 321-335.
DOI Google Scholar

Binda, C., Lopetuso, L.R., Rizzatti, G., Gibiino, G., Cennamo, V., Gasbarrini, A., 2018. Actinobacteria: A relevant minority for the maintenance of gut homeostasis. Dig. Liver Dis. 50, 421-428.
DOI Google Scholar

Bodawatta, K.H., Freiberga, I., Puzejova, K., Sam, K., Poulsen, M., Jøensson, K.A., 2021a. Flexibility and resilience of great tit (Parus major) gut microbiomes to changing diets. Anim. Microbiome. 3, 1-14.
DOI Google Scholar

Bodawatta, K.H., Hird, S.M., Grond, K., Poulsen, M., Jøensson, K.A., 2022a. Avian gut microbiomes taking flight. Trends Microbiol. 30, 268-280.
DOI Google Scholar

Bodawatta, K.H., Klečková, I., Klečka, J., Pužejová, K., Koane, B., Poulsen, M., et al. 2022b. Specific gut bacterial responses to natural diets of tropical birds. Sci. Rep. 12, 1-15.
DOI Google Scholar

Bodawatta, K.H., Koane, B., Maiah, G., Sam, K., Poulsen, M., Jønsson, K.A., 2021b. Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications. Proc. R. Soc. B. 288, 20210446.
DOI Google Scholar

Bodawatta, K.H., Sam, K., Jønsson, K.A., Poulsen, M., 2018. Comparative analyses of the digestive tract microbiota of New Guinean passerine birds. Front. Microbiol. 9, 1830.
DOI Google Scholar

Bordenstein, S.R., Theis, K.R., 2015. Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biol. 13, 1-23.
DOI Google Scholar
Borenstein, M., Hedges, L.V., Higgins, J.P.T., Rothstein, H.R., 2021. Introduction to Meta-analysis. John Wiley & Sons, Chichester.
DOI

Bradley, P.H., Pollard, K.S., 2017. Proteobacteria explain significant functional variability in the human gut microbiome. Microbiome. Microbiome, 5, 1-23.
DOI Google Scholar

Buckley, D.H., Huangyutitham, V., Nelson, T.A., Rumberger, A., Thies, J.E., 2006. Diversity of Planctomycetes in soil in relation to soil history and environmental heterogeneity. Appl. Environ. Microbiol. 72, 4522-4531.
DOI Google Scholar

Burge, M.N., 1988. Fungi in Biological Control Systems. Manchester University Press, Manchester.

Burin, G., Kissling, W.D., Guimarães, P.R., Şekercioğlu, Ç.H., Quental, T.B., 2016. Omnivory in birds is a macroevolutionary sink. Nat. Commun. 7, 1-10.
DOI Google Scholar

Capunitan, D.C., Johnson, O., Terrill, R.S., Hird, S.M., 2020. Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Mol. Ecol. 29, 829-847.
DOI Google Scholar

Chen, H., Boutros, P.C., 2011. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12, 35.
DOI Google Scholar

Chen, C.Y., Chen, C.K., Chen, Y.Y., Fang, A., Shaw, G.T.W., Hung, C.M., et al., 2020. Maternal gut microbes shape the early-life assembly of gut microbiota in passerine chicks via nests. Microbiome 8, 1-13.
DOI Google Scholar

Cho, H., Lee, W.Y., 2020. Interspecific comparison of the fecal microbiota structure in three Arctic migratory bird species. Ecol. Evol. 10, 5582-5594.
DOI Google Scholar

Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200.
DOI Google Scholar

Evans, A.D., Smith, K.W., Buckingham, D.L., Evans, J., 1997. Seasonal variation in breeding performance and nestling diet of Cirl Buntings Emberiza cirlus in England. Bird Study 44, 66-79.
DOI Google Scholar

Faith, J.J., Guruge, J.L., Charbonneau, M., Subramanian, S., Seedorf, H., Goodman, A.L., et al., 2013. The long-term stability of the human gut microbiota. Sci. Am. 341, 1237439.
DOI Google Scholar

Felice, R.N., Tobias, J.A., Pigot, A.L., Goswami, A., 2019. Dietary niche and the evolution of cranial morphology in birds. Proc. R. Soc. B-Biol. Sci. 286, 20182677. https://doi.org/10.1098/rspb.2018.2677.
DOI Google Scholar

Fu, R, Xiang, X, Dong, Y, Cheng, L, Zhou, L, 2020. Comparing the intestinal bacterial communies of sympatric wintering Hooded Crane (Grus monacha) and Domestic Goose (Anser anser domesticus). Avian Res. 11, 13. https://doi.org/10.1186/s40657-020-00195-9.
DOI Google Scholar

Gause, G.F., 1934. Experimental analysis of Vito Volterra's mathematical theory of the struggle for existence. Science 79, 16-17.
DOI Google Scholar

Góngora, E., Elliott, K.H., Whyte, L., 2021. Gut microbiome is affected by inter-sexual and inter-seasonal variation in diet for thick-billed murres (Uria lomvia). Sci. Rep. 11, 1-12.
DOI Google Scholar

Goulão, B, Santos, O, Carmo, I, 2015. The impact of migration on body weight: a review. Cad. Saude Publica. 31 (2), 229–45.
DOI Google Scholar

Greene, L.K., Williams, C.V., Junge, R.E., Mahefarisoa, K.L., Rajaonarivelo, T., Rakotondrainibe, H., et al. 2020. A role for gut microbiota in host niche differentiation. ISME J. 14, 1675-1687.
DOI Google Scholar

Grevé, ME, Houadria, M, Andersen, AN, Menzel, F, 2019. Niche differentiation in rainforest ant communities across three continents. Ecol. Evol. 9 (15), 8601–15.
DOI Google Scholar

Grond, K., Sandercock, B.K., Jumpponen, A., Zeglin, L.H., 2018. The avian gut microbiota: community, physiology and function in wild birds. J. Avian Biol. 49, e01788.
DOI Google Scholar

Hird, S.M., Sánchez, C., Carstens, B.C., Brumfield, R.T., 2015. Comparative gut microbiota of 59 neotropical bird species. Front. Microbiol. 1403.
DOI Google Scholar

Hou, X, Pan, S, Lin, Z, Xu, J, Zhan, X, 2021. Performance comparison of different microbial DNA extraction methods on bird feces. Avian Res .12, 19. https://doi.org/10.1186/s40657-021-00254-9.
DOI Google Scholar

Hrdina, A., Romportl, D., 2017. Evaluating global biodiversity hotspots-very rich and even more endangered. J. Landsc. 10, 108-115.
DOI Google Scholar

Hsiung, A.C., Boyle, W.A., Cooper, R.J., Chandler, R.B., 2018. Altitudinal migration: ecological drivers, knowledge gaps, and conservation implications. Biol. Rev. 93, 2049-2070.
DOI Google Scholar

Huang, K, Wang, J, Huang, J, Zhang, S, Vogler, AP, Liu, Q, et al., 2021. Host Phylogeny and Diet Shape Gut Microbial Communities Within Bamboo-Feeding Insects. Front. Microbiol. 12, 633075. https://doi.org/10.3389/fmicb.2021.633075.
DOI Google Scholar

Hyslop, E.J., 1980. Stomach contents analysis-a review of methods and their application. J. Fish Biol. 17, 411-429.
DOI Google Scholar

Jetz, W., Thomas, G.H., Joy, J.B., Hartmann, K., Mooers, A.O., 2012. The global diversity of birds in space and time. Nature 491, 444-448.
DOI Google Scholar

Kashinskaya, E.N., Belkova, N.L., Izvekova, G.I., Simonov, E.P., Andree, K.B., Glupov, V.V., et al., 2015. A comparative study on microbiota from the intestine of Prussian carp (Carassius gibelio) and their aquatic environmental compartments, using different molecular methods. J. Appl. Microbiol. 119, 948-961.
DOI Google Scholar

Kelly, D., King, T., Aminov, R., 2007. Importance of microbial colonization of the gut in early life to the development of immunity. Mutat. Res. Mol. Mech. Mutagen. 622, 58-69.
DOI Google Scholar

Kuczynski, J., Stombaugh, J., Walters, W.A., González, A., Caporaso, J.G., Knight, R., 2012. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr. Protoc. Microbiol. https://doi.org/10.1002/0471250953.bi1007s36.
DOI Google Scholar

Laparra, JM, Sanz, Y, 2010. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol. Res. 61 (3), 219–25.
DOI Google Scholar

Ley, R.E., Lozupone, C.A., Hamady, M., Knight, R., Gordon, J.I., 2008. Worlds within worlds: Evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6, 776-788.
DOI Google Scholar

Li, T., Long, M., Li, H., Gatesoupe, F.J., Zhang, X., Zhang, Q., et al. 2017. Multi-omics analysis reveals a correlation between the host phylogeny, gut microbiota and metabolite profiles in cyprinid fishes. Front. Microbiol. 8, 1-11.
DOI Google Scholar

Magoč, T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963.
DOI Google Scholar

Miyake, S, Ngugi, DK, Stingl, U, 2015. Diet strongly influences the gut microbiota of surgeonfishes. Mol. Ecol. 24 (3), 656–72.
DOI Google Scholar

Morimoto, G., Yamaguchi, N., Ueda, K., 2006. Plumage color as a status signal in male-male interaction in the red-flanked bushrobin, Tarsiger cyanurus. J. Ethol. 24, 261-266.
DOI Google Scholar

Muegge, B.D., Kuczynski, J., Knights, D., Clemente, J.C., González, A., Fontana, L., et al., 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970-974.
DOI Google Scholar

Pan, D., Yu, Z., 2014. Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes 5, 108-119.
DOI Google Scholar
Pianka, E.R., 2011. Evolutionary Ecology. seventh edition. eBook.

Pourabedin, M., Zhao, X., 2015. Prebiotics and gut microbiota in chickens. FEMS Microbiol. Lett. 362, 1-8.
DOI Google Scholar

Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al., 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-596.
DOI Google Scholar

Richardson, KC, Wooller, RD, 1986. The structures of the gastrointestinal tracts of honeyeaters and other small birds in relation to their diets. Aust. J. Zool. 34 (2), 119–24.
DOI Google Scholar

Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584.
DOI Google Scholar

Sangster, G., Alström, P., Forsmark, E., Olsson, U., 2010. Multi-locus phylogenetic analysis of Old World chats and flycatchers reveals extensive paraphyly at family, subfamily and genus level (Aves: Muscicapidae). Mol. Phylogenet. 57, 380-392.
DOI Google Scholar

Schoener, T.W., 1974. Resource partitioning in ecological communities. Science 185, 27-39.
DOI Google Scholar

Stanley, D., Geier, M.S., Hughes, R.J., Denman, S.E., Moore, R.J., 2013. Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One 8, 6-12.
DOI Google Scholar

Thomas, F., Hehemann, J.H., Rebuffet, E., Czjzek, M., Michel, G., 2011. Environmental and gut Bacteroidetes: The food connection. Front. Microbiol. 2, 1-16.
DOI Google Scholar

Tomczak, M., Tomczak, E., 2014. The need to report effect size estimates revisited. An overview of some recommended measures of effect size. Trends Sport Sci. 1, 19-25.
Google Scholar

Wang, W., Gao, X., Zheng, S., Lancuo, Z., Li, Y., Zhu, L., et al. 2021a. The gut microbiome and metabolome of Himalayan Griffons (Gyps himalayensis): insights into the adaptation to carrion-feeding habits in avian scavengers. Avian Res. 12, 52.
DOI Google Scholar

Wang, W., Zhou, L., Fu, R., Cheng, L., Yan, S., Mahtab, N., et al., 2021b. Effects of foraging site distances on the intestinal bacterial community compositions of the sympatric wintering Hooded Crane (Grus monacha) and Domestic Duck (Anas platyrhynchos domesticus). Avian Res. 12, 20.
DOI Google Scholar

Whelan, CJ, Şekercioğlu, ÇH, Wenny, DG, 2015. Why birds matter: from economic ornithology to ecosystem services. J. Ornithol. 156, 227–38.
DOI Google Scholar

Wilman, H., Belmaker, J., Simpson, J., de la Rosa, C., Rivadeneira, M.M., Jetz, W., 2014. EltonTraits 1.0 : Species-level foraging attributes of the world's birds and mammals. Ecology 95, 2027.
DOI Google Scholar

Wu, Y, DuBay, SG, Colwell, RK, Ran, J, Lei, F, 2017. Mobile hotspots and refugia of avian diversity in the mountains of south-west China under past and contemporary global climate change. J. Biogeogr. 44 (3), 615–26.
DOI Google Scholar

Xiang, B, Zhao, L, Zhang, M, 2021. Metagenome-scale metabolic network suggests folate produced by bifidobacterium longum might contribute to high-fiber-diet-induced weight loss in a prader–willi syndrome child. Microorganisms 9, 2493. https://doi.org/10.3390/microorganisms9122493.
DOI Google Scholar

Xiao, F, Zhu, W, Yu, Y, He, Z, Wu, B, Wang, C, et al., 2021. Host development overwhelms environmental dispersal in governing the ecological succession of zebrafish gut microbiota. npj Biofilms Microbiomes 7, 5. https://doi.org/10.1038/s41522-020-00176-2.
DOI Google Scholar

Youngblut, N.D., Reischer, G.H., Walters, W., Schuster, N., Walzer, C., Stalder, G., et al., 2019. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10, 1-15.
DOI Google Scholar

Zhang, YJ, Li, S, Gan, RY, Zhou, T, Xu, DP, Li, H Bin, 2015. Impacts of gut bacteria on human health and diseases. Int. J. Mol. Sci. 16 (4), 7493–519.
DOI Google Scholar

Zu, K., Luo, A., Shrestha, N., Liu, B., Wang, Z., Zhu, X., 2019. Altitudinal biodiversity patterns of seed plants along Gongga Mountain in the southeastern Qinghai-Tibetan Plateau. Ecol. Evol. 9, 9586-9596.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 24 April 2022
Revised: 05 July 2022
Accepted: 11 July 2022
Published: 19 July 2022
Issue date: September 2022

Copyright

© 2022 The Authors.

Acknowledgements

Acknowledgements

We thank Zhengwei Liu, Xiaofeng Zheng, Kaize Feng, Yanni Zhang, Kexin Peng for their kind assistance with fieldwork and data collection. We thank Faming Liu and Quanxiao Lan at Gongga Alpine Ecosystem Observation and Research Station for their kind assistance with the fieldwork. We thank Nanjiong Pang and Dongrui Li for their advice and assistance during the writing of the manuscript. This study was financially supported by The Second Tibetan Plateau Scientific Expedition and Research Program (No. 2019QZKK0501) and National Natural Science Foundation of China (No. 31772478, 31501851).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return