Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Tao Liu, Yongtao Xu, Canwei Xia, David Edwards, Xiaolong Hu, Yingyu Su, Jinsheng Xie, Weiwei Zhang. 2022: Multiple lines of evidence confirm that the critically endangered Blue-crowned Laughingthrush (Garrulax courtoisi) is an independent species. Avian Research, 13(1): 100022. doi: 10.1016/j.avrs.2022.100022
Citation: Tao Liu, Yongtao Xu, Canwei Xia, David Edwards, Xiaolong Hu, Yingyu Su, Jinsheng Xie, Weiwei Zhang. 2022: Multiple lines of evidence confirm that the critically endangered Blue-crowned Laughingthrush (Garrulax courtoisi) is an independent species. Avian Research, 13(1): 100022. doi: 10.1016/j.avrs.2022.100022

Multiple lines of evidence confirm that the critically endangered Blue-crowned Laughingthrush (Garrulax courtoisi) is an independent species

doi: 10.1016/j.avrs.2022.100022
More Information
  • The taxonomy of the Blue-crowned Laughingthrush (Garrulax courtoisi) and its relationship with the Yellow-throated Laughingthrush (G. galbanus) and G. c. simaoensis, a range-restricted subspecies in China, has not been fully elucidated. So the taxonomic status and system evolution of the three taxa G. courtoisi, G. galbanus and G. c. simaoensis need to be reclarified. Two gene sequences myoglobin (MYO) and the mitochondrial cytochrome coxidase subunit I (COI) were combined to investigate the phylogenetic relationships among courtoisi, simaoensis and galbanus, genetic data, combining with morphological, ecological and acoustic data were used to comb out the classification status and divergence level of the three taxa. Significant genetic and morphological differentiations (body size and plumage coloration) were detected between courtoisi and galbanus. However, no notable and reliable differences between the courtoisi and simaoensis were detected. The courtoisi, simaoensis and galbanus are clearly isolated in geographical distribution as a result of differing altitudes, climate conditions and habitats. The courtoisi has characteristic preference for nest location compared with galbanus. In addition, the results of song analysis also indicated that there are differences in maximum frequency between courtoisi and galbanus. G. courtoisi was confirmed to be an independent species based on genetic, morphological, geographical, ecological and vocal characteristics, and the validity of simaoensis as a subspecies still need more evidence. This study further confirmed the high conservation value of Blue-crowned Laughingthrush. In addition, due to the genetic differences between Simao and Wuyuan populations, this should be fully considered in future protection strategies.


  • loading
  • Alström, P.F., Rheindt, E., Zhang, R., Zhao, M., Wang, J., Zhu, J., et al., 2018. Complete species-level phylogeny of the leaf warbler (Aves: Phylloscopidae) radiation. Mol. Phylogenet. Evol. 126, 141-152. https://doi.org/10.1016/j.ympev.2018.03.031.
    Ashton, K.G., 2002. Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule. Global Ecol. Biogeogr. 11, 505-523. https://doi.org/10.1046/j.1466-822X.2002.00313.x.
    Baker, E.C.S., 1894. The birds of North Cachar. Bombay Nat. Hist. Soc. 8, 162-211.
    Baker, E.C.S., 1932. The Nidification of Birds of the Indian Empire, 1. Taylor and Francis, London.
    Bergmann, C., 1847. About the relationships between heat conservation and body size of animals. Goett. Stud. 1, 595-708.
    Berlioz, J., 1930. Révision systématique du genre Garrulax lesson. L' Oiseau 11, 1-9.
    BirdLife International, 2018. Garrulax courtoisi. The IUCN Red List of Threatened Species 2018: e. T22732350A131890764. https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22732350A131890764.en. (accessed 02 March 2022).
    Cai, T., Cibois, A., Alström, P., Moyle, R.G., Kennedy, J.D., Shao, S., et al., 2019. Near-complete phylogeny and taxonomic revision of the world's babblers (Aves: Passeriformes). Mol. Phylogenet. Evol. 130, 346-356. https://doi.org/10.1016/j.ympev.2018.10.010.
    Cheng, S., Lin, J., 2011. A survey on avian diversity in Wuyishan National Nature Reserve, Jiangxi. Chin. J. Zool. 46, 66-78. (in Chinese).
    Cheng, T., Tang, R., 1982. A new subspecies of Garrulax galbanus from Yunnan, China. Sinozoologica. 2, 1-2.
    Cibois, A., Gelang, M., Alström, P., Pasquet, E., Fjeldså, J., Ericson, P.G.P., et al., 2018. Comprehensive phylogeny of the laughingthrushes and allies (Aves, Leiothrichidae) and a proposal for a revised taxonomy. Zool. Scr. 1, 1-13. https://doi.org/10.1111/zsc.12296.
    Collar, N.J., 2006. A partial revision of the Asian babblers (Timaliidae). Forktail 22, 85-112. https://citeseerx.ist.psu.edu/viewdoc/download?doi=
    Collar, N.J., Robson, C., 2007. Family Timaliidae (babblers). In: del Hoyo, J., Elliott, A., Christie, D.A., (Eds. ), Handbook of the Birds of the World, 12. Lynx Edicions, Barcelona, pp. 70-291.
    del Hoyo, J., Collar, N.J., 2016. HBW and BirdLife International Illustrated Checklist of the Birds of the World. Volume 2: Passerines. Lynx Edicions and BirdLife International, Barcelona.
    Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973. https://doi.org/10.1093/molbev/mss075.
    Edwards, D.P., Borah, J., Eaton, J.A., 2016. First description of the song of Yellow-throated Laughingthrush Garrulax (Dryonastes) galbanus, Nagaland, north-east India. BirdingASIA 25, 87-88. https://www.researchgate.net/publication/305983914_First_description_of_the_song_of_Yellow-throated_Laughingthrush_Garrulax_Dryonastes_galbanus_Nagaland_north-east_India
    Etchecopar, R.D., Hue, F., 1983. Les oiseaux de Chine, de Mongolie et de Coree: Passereaux. Editions du Pacifique, Papeete.
    Gelang, M., Cibois, A., Pasquet, E., Olsson, E., Alström, P., Ericson, P.G., 2009. Phylogeny of babblers (Aves, Passeriformes): major lineages, family limits and classification. Zool. Scr. 38, 225-236. https://doi.org/10.1111/j.1463-6409.2008.00374.x.
    Gill, F., Donsker, D., Rasmussen, P., 2022. IOC World Bird List (v 12.1). http://www.worldbirdnames.org/. (accessed 15 January 2022).
    Godwin-Austen, H.H., 1874. Descriptions of ten new birds from the Nágá hills and munipúr valley, N.E. Frontier of Bengal. Proc. Zool. Soc. London 42, 43-48. https://doi.org/10.1111/j.1096-3642.1874.tb02450.x.
    Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwtchs, W., Hebert, P.D.N., 2006. DNA barcodes distinguish species of tropical Lepidoptera. P. Natl. Acad. Sci. U. S. A. 103, 968-971. https://doi.org/10.1073/pnas.0510466103.
    He, F.Q., Yang, L., 2006. The new discussion on the classification of the G. courtoisi. Chin. J. Zool. 41, 127.
    He, F.Q., Lin, J.S., Gardner, J., Richardson, M., Wilkinson, R., 2007. Searches for the Blue-crowned Laughingthrush Garrulax courtoisi simaoensis in south Yunnan, south-west China. Avicult. Mag. 113, 78-84. https://www.biodiversitylibrary.org/part/314939
    He, F.Q., Lin, J.S., Wen, C., Lin, Z., Shi, Q.H., Huang, H.Q., et al., 2017. Prelim of biology of the Blue-crowned Laughingthrush Garrulax courtoisi in Wuyuan of NE Jiangxi, SE China. Chin. J. Zool. 52, 167-175. (in Chinese). https://en.cnki.com.cn/Article_en/CJFDTOTAL-BIRD201701023.htm
    Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M., 2004. Identification of birds through DNA barcodes. PLoS Biol. 2, 1657-1663.
    Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature 405, 907-913. doi: 10.1038/35016000
    Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philos. T. Roy. Soc. B. 359, 183-195. doi: 10.1098/rstb.2003.1388
    Hong, D.Y., 2016. Biodiversity pursuits need a scientific and operative species concept. Biodivers. Sci. 24, 979-999. doi: 10.17520/biods.2016203
    Hong, Y., He, F.Q., Roland, W., Melaille, D., Zheng, P., 2003. Little-known oriental bird Courtois's Laughingthrush Garrulax galbanus courtoisi. Orient. Bird Club 38, 35-39.
    Hong, Y.H., Yu, S., Liao, W., 2006. A Study on the breeding habitat of Garrulax galbanus courtoisi in Wuyuna, Jiangxi Province. Acta Agr. Univ. Jiangxi. 28, 907-911. https://doi.org/10.3969/j.issn.1000-2286.2006.06.023 (in Chinese).
    Hopwood, J.C., Mackenzie, J.M.D., 1917. A list of birds from the North Chin Hills. J. Bombay Nat. Hist. Soc. 25, 72-91.
    Huang, H.Q., Liu, T., Shi, J.Z., Liu, P., Zhang, W.W., 2018. Habitat selection of the Blue-Crowned Laughingthrush during the breeding season. Acta Ecol. Sin. 38, 493-501. https://doi.org/10.5846/stxb201609261942 (in Chinese).
    Hume, A.O., 1888. The birds of Manipur, Assam, Sylhet and Cachar. Stray Feathers 11, 1-353. https://pubs.geoscienceworld.org/sgf/bsgf/article-abstract/175/4/413/123027/The-birds-of-the-Djurab-Pliocene-faunas-Chad
    Inskipp, T., Lindsey, N., Duckworth, W., 1996. An Annotated Checklist of the Birds of the Oriental Region. The Oriental Bird Club, Sandy.
    Irestedt, M., Ohlson, J.I., Zuccon, D., Kallersjo, M., Ericson, P.G.P., 2006. Nuclear DNA from old collections of avian study skins reveals the evolutionary history of the Old World Suboscines (Aves, Passeriformes). Zool. Scr. 35, 567-580. https://doi.org/10.1111/j.1463-6409.2006.00249.x.
    Irestedt, M., Batalha-Filho, H., Roselaar, C.S., Christidis, L., Ericson, P.G.P., 2016. Contrasting phylogeographic signatures in two Australo-Papuan bowerbird species complexes (Aves: Ailuroedus). Zool. Scr. 45, 365-379. https://doi.org/10.1111/zsc.12163.
    Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549. https://doi.org/10.1093/molbev/msy096.
    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., Calcott, B., 2016. Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772-773. https://doi.org/10.1093/molbev/msw260.
    Lavinia, P.D., Kerr, K.C.R., Tubaro, P.L., Hebert, P.D.N., Lijtmaer, D.A., 2016. Calibrating the molecular clock beyond cytochrome b: assessing the evolutionary rate of COI in birds. J. Avian Biol. 47, 84-91. doi: 10.1111/jav.00766
    Li, N., Huang, X.L., Yan, Q., Zhang, W.W., Wang, Z., 2021. Save China's blue-crowned laughingthrush. Science 373, 171. doi: 10.1126/science.abj4535
    Liu, J.Q., 2016. "The integrative species concept" and "species on speciation way". Biodivers. Sci. 24, 1004-1008. https://doi.org/10.17520/biods.2016222. (in Chinese).
    Liu, T., Xu, Y.T., Mo, B., Shi, J.Z., Cheng, Y.C., Zhang, W.W., et al., 2020. Home range size and habitat use of the Blue-crowned Laughingthrush during the breeding season. PeerJ 8, e8785. http://doi.org/10.7717/peerj.8785.
    Long, A., Crosby, M., Inskipp, T., 1994. A review of the taxonomic status of the Yellow-throated Laughingthrush Garrulax galbanus. Orient. Bird Club 19, 41-48.
    Luo, X., Qu, Y.H., Han, L., Li, S., Lei, F.M., 2008. A phylogenetic analysis of laughingthrushes (Timaliidae: Garrulax) and allies based on mitochondrial and nuclear DNA sequence. Zool. Scr. 38, 9-22. https://doi.org/10.1111/j.1463-6409.2008.00355.x.
    MacKinnon, J., Phillipps, K., He, F.Q., 2000. A Field Guide to the Birds of China. Hunan Education Press, Changsha, China. (in Chinese).
    Ménégaux, A., 1923. Description du Garrulax courtoisi, nov. sp. De la Chine. Bull. Mus. Hist. Nat. 29, 287-288.
    Nguyen, L.T., Schmidt, H.A., Haeseler, A., Minh, B.Q., 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol. 32, 268-274. https://doi.org/10.1111/j.1463-6409.2008.00355.x.
    Pasini, A., Arsuffi, D., Micali, G., Violani, C.G., 1994. Identification and captive breeding of the Yellow-throated Laughingthrush Garrulax galbanus simaoensis in northern Italy. Orient. Bird Club Bull. 19, 49-50.
    Rambaut, A., 2018. Fig tree v1.4.4. http://tree.bio.ed.ac.uk/software/fig–tree. (accessed 10 May 2021).
    Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J., 2018. Tracer v1.7.1. http://beast.bio.ed.ac.uk/tracer. (accessed 10 May 2021).
    Rao, P.C., 1996. Study on the woody plant flora in Wuyuan County. J. Nanjing Forest. Univ. 20, 84–87 (in Chinese).
    Ripley, S.D., 1952. A collection of birds from the Naga Hills. J. Bombay Nat. Hist. Soc. 50, 475-514. https://www.biodiversitylibrary.org/part/153546
    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542. https://doi.org/10.1093/sysbio/sys029.
    Singh, N.D., Yadav, R.R., Venugopal, N., Singh, T.B., Sanjita, C., Yadava, A.K., et al., 2016. Climate control on ring width and intra-annual density fluctuations in Pinus kesiya growing in a sub-tropical forest of Manipur, Northeast India. Trees (Berl.) 30, 1711-1721. https://doi.org/10.1007/s00468-016-1402-9.
    Song, F., Zhao, J., Zhang, Y., Xu, Z., Xiao, L., 2010. Impact of regional climate change on plant growth trend in Xishuangbanna. Acta Bot. Yunnanica 32, 547-553. https://doi.org/10.3724/SP.J.1143.2010.10140.
    Thompson, P.M., Harvey, W.G., Johnson, D.L., 1993. Recent notable bird records from Bangladesh. Forktail 9, 13-44.
    Touchton, J.M., Seddon, N., Tobias, J.A., 2014. Captive rearing experiments confirm song development without learning in a tracheophone suboscine bird. PloS ONE 9, e95746. https://doi.org/10.1371/journal.pone.0095746.
    Wang, Z., Chen, J., Deng, X., Bai, Z., Yang, Q., Liu, Y., 2000. Morus macroura and the wildlife who eat his berry in different mountain regions, Xishuangbanna, Yunnan J. Mount. Sci. 18, 267-271. (in Chinese).
    Wilkinson, R., He, F.Q., 2010a. Yellow-throated Laughingthrush Garrulax galbanus and Blue-crowned Laughingthrush G. courtoisi new observations and interpretations on their taxonomy. BirdingASIA 14, 73-82.
    Wilkinson, R., He, F.Q., 2010b. Conservation of Blue-crowned Laughingthrush Garrulax courtoisi in Wuyuan, Jiangxi, and the search for 'lost' populations in Yunnan and Guangxi, China. BirdingASIA 13, 100-105.
    Wilkinson, R., He, F.Q., Gardner, L., 2004. A highly threatened bird-Chinese Yellow-throated Laughingthrushes in China and in zoos. Int. Zoo News 51, 456-469.
    Zhang, W.W., Shi, J.Z., Huang, H.Q., Liu, T., 2017. The impact of disturbance from photographers on the Blue-crowned Laughingthrush (Garrulax courtoisi). Avian Conserv. Ecol. 12, 1. https://doi.org/10.5751/ACE-01007-120115.
    Zheng, Z., Zheng, B., 1962. On birds from Hsi-Shuan-Pan-Na area and vicinity in Yunnan Province. Ⅲ. Acta Zool. Sin. 14, 74-94. (in Chinese).
    Zhu, H., Wang, H., Li, B., Zhou, S., Zhang, J., 2015. Study on Xishuangbanna Forest Vegetation. J. Plant Sci. 33, 641-726. https://doi.org/10.11913/PSJ.2095-0837.2015.50641.
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(4)

    Article Metrics

    Article views (42) PDF downloads(2) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint