Volume 12 Issue 1
Jul.  2021
Turn off MathJax
Article Contents
Abstract
References
Related Articles
Charlotte E. Hacker, Brandon D. Hoenig, Liji Wu, Wei Cong, Wei Cong, Jingjing Yu, Yunchuan Dai, Ye Li, Jia Li, Yadong Xue, Yu Zhang, Yunrui Ji, Hanning Cao, Diqiang Li, Yuguang Zhang, Jan E. Janecka. 2021: Use of DNA metabarcoding of bird pellets in understanding raptor diet on the Qinghai-Tibetan Plateau of China. Avian Research, 12(1): 42. DOI: 10.1186/s40657-021-00276-3
Citation: Charlotte E. Hacker, Brandon D. Hoenig, Liji Wu, Wei Cong, Wei Cong, Jingjing Yu, Yunchuan Dai, Ye Li, Jia Li, Yadong Xue, Yu Zhang, Yunrui Ji, Hanning Cao, Diqiang Li, Yuguang Zhang, Jan E. Janecka. 2021: Use of DNA metabarcoding of bird pellets in understanding raptor diet on the Qinghai-Tibetan Plateau of China. Avian Research, 12(1): 42. DOI: 10.1186/s40657-021-00276-3
shu

Use of DNA metabarcoding of bird pellets in understanding raptor diet on the Qinghai-Tibetan Plateau of China

  • 1.

    Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, and Key Laboratory of Biodiversity Protection of National Forestry and Grassland Administration, Beijing 100091, China

  • 2.

    Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282, USA

  • 3.

    Yanchiwan National Nature Reserve of Gansu Province, Subei 736300, China

  • 4.

    Institute for Ecology and Environmental Resources, Chongqing Academy of Social Sciences, Chongqing 400020, China

  • 5.

    The High School Affiliated to Renmin, University of China, Beijing 100872, China

More Information
  • Corresponding author:

    Yuguang Zhang, E-mail:yugzhang@sina.com

    Jan E. Janecka, E-mail:janeckaj@duq.edu

  • Received Date: 25 Feb 2021
  • Accepted Date: 31 Jul 2021
  • Available Online: 24 Apr 2022
  • Publish Date: 20 Aug 2021
    Graphical Abstract
    • Abstract
  • Background 

    Diet analysis is essential to understanding the functional role of large bird species in food webs. Morphological analysis of regurgitated bird pellet contents is time intensive and may underestimate biodiversity. DNA metabarcoding has the ability to circumvent these issues, but has yet to be done.

    Methods 

    We present a pilot study using DNA metabarcoding of MT-RNR1 and MT-CO1 markers to determine the species of origin and prey of 45 pellets collected in Qinghai and Gansu Provinces, China.

    Results 

    We detected four raptor species [Eurasian Eagle Owl (Bubo bubo), Saker Falcon (Falco cherrug), Steppe Eagle (Aquila nipalensis), and Upland Buzzard (Buteo hemilasius)] and 11 unique prey species across 10 families and 4 classes. Mammals were the greatest detected prey class with Plateau Pika (Ochotona curzoniae) being the most frequent. Observed Shannon's and Simpson's diversity for Upland Buzzard were 1.089 and 0.479, respectively, while expected values were 1.312±0.266 and 0.485±0.086. For Eurasian Eagle Owl, observed values were 1.202 and 0.565, while expected values were 1.502±0.340 and 0.580±0.114. Interspecific dietary niche partitioning between the two species was not detected.

    Conclusions 

    Our results demonstrate successful use of DNA metabarcoding for understanding diet via a novel noninvasive sample type to identify common and uncommon species. More work is needed to understand how raptor diets vary locally, and the mechanisms that enable exploitation of similar dietary resources. This approach has wide ranging applicability to other birds of prey, and demonstrates the power of using DNA metabarcoding to study species noninvasively.

    • FullText(HTML)

  • Correction to: Avian Res (2021) 12:19

    https://doi.org/10.1186/s40657-021-00254-9

    Following publication of the original article (Hou et al. 2021), the authors identified an error in Fig. 1. The correct figure is given below.

    Figure  1.  The experiment design in this study
    DownLoad: Full-Size Img PowerPoint

    The original article (Hou et al. 2021) has been updated.

    • References (85)
  • Avery ML, Cummings JL. Livestock depredations by black vultures and golden eagles. Sheep Goat Res J. 2004;19: 58-63.
    Badingqiuying, Smith AT, Senko J, Siladan MU. Plateau pika Ochotona curzoniae poisoning campaign reduces carnivore abundance in southern Qinghai, China. Mammal Study. 2016;41: 1-8.
    Birdlife International. Bubo bubo (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017: e. T22688927A113569670. 2017. .
    Birdlife International. Falco cherrug (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017: e. T22696495A110525916. 2018a. .
    Birdlife International. Buteo hemilasius. The IUCN Red List of Threatened Species 2018: e. T22695967A131937792. 2018b. .
    Birdlife International. Aquila nipalensis (amended version of 2017 assessment). The IUCN Red List of Threatened Species 2019: e. T22696038A155419092. 2019. .
    Bontzorlos VA, Peris SJ, Vlachos CG, Bakaloudis DE. The diet of barn owl in the agricultural landscapes of central Greece. Folia Zool. 2005;54: 99-110.
    Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E. Obitools: a unix-inspired software package for DNA metabarcoding. Mol Ecol Resour. 2016;16: 176-82.
    Chen D, Zhang X, Tan X, Wang K, Qiao Y, Chang Y. Hydroacoustic study of spatial and temporal distribution of Gymnocypris przewalskii (Kessler, 1876) in Qinghai Lake, China. Environ Biol Fish. 2009;84: 231-9.
    Cui Q, Su J, Jiang Z. Summer diet of two sympatric species of raptors Upland Buzzard (Buteo hemilasius) and Eurasian Eagle Owl (Bubo bubo) in alpine meadow: problem of coexistence. Pol J Ecol. 2008;56: 173-9.
    Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, et al. Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data? Mol Ecol. 2019;28: 391-406.
    Dixon A, Maming R, Gunga A, Purev-Ochir G, Batbayar N. The problem of raptor electrocution in Asia: case studies from Mongolia and China. Bird Conserv Int. 2013;23: 520-9.
    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32: 1792-7.
    Emmrich M, Düttmann H. Seasonal shifts in diet composition of Great Cormorants Phalacrocorax carbo sinensis foraging at a shallow eutrophic inland lake. Ardea. 2011;99: 207-16.
    Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, et al. Trophic downgrading of planet earth. Science. 2011;333: 301-6.
    Ewins PJ, Weseloh DV, Groom JH, Dobos RZ, Mineau P. The diet of Herring Gulls (Larus argentatus) during winter and early spring on the lower Great Lakes. Hydrobiologia. 1994;279(280): 39-55.
    Foggin JM. Depopulating the Tibetan grasslands: national policies and perspectives for the future of Tibetan herders in Qinghai Province, China. Mt Res Dev. 2008;28: 26-31.
    Freeland JR. The importance of molecular markers and primer design when characterizing biodiversity from environmental DNA. Genome. 2017;60: 358-74.
    Galan M, Pagès M, Cosson JF. Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS ONE. 2012;7: e48374.
    Gotelli NJ, Hart EM, Ellison AM. EcoSimR: null model analysis for ecological data. R Package version 0.1.0. 2015. .
    Granjon L, Bruderer C, Cosson JF, Dia AT, Colas F. The small mammal community of a coastal site of south-west Mauritania. Afr J Ecol. 2002;40: 10-7.
    Grier JW. Ban of DDT and subsequent recovery of reproduction in bald eagles. Science. 1982;218: 1232-5.
    Guimaraes S, Fernandez-Jalvo Y, Stoetzel E, Gorgé O, Bennett EA, Denys C, et al. Owl pellets: a wise DNA source for small mammal genetics. J Zool. 2016;298: 64-74.
    Hacker CE, Jevit M, Hussain S, Muhammad G, Munkhtsog B, Munkhtsog B, et al. Regional comparison of snow leopard (Panthera uncia) diet using DNA metabarcoding. Biodivers Conserv. 2021;30: 797-817.
    Hebert PDN, Cywinska A, Ball SL, deWaard JR. Biological identifications through DNA barcodes. Proc R Soc B Biol Sci. 2003;270: 313-21.
    Heck KL, van Belle G, Simberloff D. Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology. 1975;56: 1459-61.
    Hill MO. Diversity and evenness: a unifying notation and its consequences. Ecology. 1973;54: 427-32.
    Hiraldo F, Andrada J, Parreño F. Diet of the eagle owl (Bubo bubo) in Mediterranean Spain. Doñana Acta Vertebr. 1975;2: 161-77.
    Hsieh TC, Ma KH, Chao A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Method Ecol Evol. 2016;7: 1451-6.
    Hurlbert SH. The nonconcept of species diversity: a critique and alternative parameters. Ecology. 1971;52: 577-86.
    Iverson SJ, Springer AM, Kitaysky AS. Seabirds as indicators of food web structure and ecosystem variability: qualitative and quantitative diet analyses using fatty acids. Mar Ecol Prog Ser. 2007;352: 235-44.
    Jackson R. Fostering community-based stewardship of wildlife in Central Asia: transforming snow leopards from pests into valued assets. In: Squires VR, editor. Rangeland stewardship in Central Asia. Dordrecht: Springer; 2012. p. 357-80.
    Janečka JE, Jackson R, Yuquang Z, Diqiang L, Munkhtsog B, Buckley-Beason V, et al. Population monitoring of snow leopards using noninvasive collection of scat samples: a pilot study. Anim Conserv. 2008;11: 401-11.
    Janečka JE, Munkhtsog B, Jackson RM, Naranbaatar G, Mallon DP, Murphy WJ. Comparison of noninvasive genetic and camera-trapping techniques for surveying snow leopards. J Mammal. 2011;92: 771-83.
    Jedlicka JA, Vo ATE, Almeida RPP. Molecular scatology and high-throughput sequencing reveal predominately herbivorous insects in the diets of adult and nestling Western Bluebirds (Sialia mexicana) in California vineyards. Auk. 2017;134: 116-27.
    Kartzinel TR, Chen PA, Coverdale TC, Erickson DL, Kress WJ, Kuzmina ML, et al. DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc Natl Acad Sci USA. 2015;112: 8019-24.
    Lai CH, Smith AT. Keystone status of plateau pikas (Ochotona curzoniae): effect of control on biodiversity of native birds. Biodivers Conserv. 2003;12: 1901-12.
    Lamb PD, Hunter E, Pinnegar JK, Creer S, Davies RG, Taylor MI. How quantitative is metabarcoding: a meta-analytical approach. Mol Ecol. 2019;28: 420-30.
    Lei F. A study on diet of the Little Owl (Athene noctua plumipes) in Qishan, Shanxi Province, China. Wuyi Sci J. 1995;12: 136-42 (in Chinese).
    Li L, Yi X, Li M, Zhang X. Diet composition of upland buzzard: analysis on stomach content and food pellet. Zool Res. 2004;25: 162-5 (in Chinese).
    Liu X, Chen B. Climatic warming in the Tibetan Plateau during recent decades. Int J Climatol. 2000;20: 1729-42.
    Liu Y. International hunting and the involvement of local people, Dulan, Qinghai, People's Republic of China. Master's Thesis. Missoula: University of Montana; 1993.
    Marchesi L, Pedrini P, Sergio F. Biases associated with diet study methods in the Eurasian Eagle-Owl. J Raptor Res. 2002;36: 11-6.
    Margalida A, Bertran J, Boudet J. Assessing the diet of nestling Bearded Vultures: a comparison between direct observation methods. J Field Ornithol. 2005;76: 40-5.
    Margalida A, Bertran J, Heredia R. Diet and food preferences of the endangered Bearded Vulture Gypaetus barbatus: a basis for their conservation. Ibis. 2009;151: 235-43.
    Meusnier I, Singer GAC, Landry JF, Hickey DA, Hebert PDN, Hajibabaei M. A universal DNA mini-barcode for biodiversity analysis. BMC Genomics. 2008;9: 214.
    Miller C, McEwen L. Diet of nesting Savannah Sparrows in interior Alaska. J Field Ornithol. 1995;66: 152-8.
    Miller DJ, Bedunah DJ. Rangelands of the Kunlun Mountains in Western China. Rangelands. 1994;16: 71-6.
    Moody T. A method for obtaining food samples from insectivorous birds. Auk. 1970;87: 579.
    Musser GG, Carleton MD. Superfamily Muroidea. In: Wilson D, Reeder D, editors. Mammal species of the world: a taxonomic and geographic reference. 3rd ed. Baltimore: John Hopkins University; 2005. p. 894-1531.
    Oehm J, Thalinger B, Eisenkölbl S, Traugott M. Diet analysis in piscivorous birds: what can the addition of molecular tools offer? Ecol Evol. 2017;7: 1984-95.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. Package vegan: community ecology package. R Package. version 2.3-1. 2013.
    Pianka ER. Niche overlap and diffuse competition. Proc Natl Acad Sci USA. 1974;71: 2141-5.
    Pimm SL, Russell GJ, Gittleman JL, Brooks TM. The future of biodiversity. Science. 1995;269: 347-50.
    Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P. Who is eating what: diet assessment using next generation sequencing. Mol Ecol. 2012;21: 1931-50.
    Rasmussen P, Anderson J. Birds of South Asia: the ripley guide. Washington, DC, and Barcelona: Smithsonian Institution and Lynx Edicions; 2005.
    Reading R, Michel S, Amgalanbaatar S. Ovis ammon. The IUCN Red List of Threatened Species 2020: e. T15733A22146397. 2020. .
    Riaz T, Shehzad W, Viari A, Pompanon F, Taberlet P, Coissac E. ecoPrimers: inference of new DNA barcode markers from whole genome sequence analysis. Nucleic Acids Res. 2011;39: e145.
    Sándor AD, Ionescu DT. Diet of the eagle owl (Bubo bubo) in Braşov, Romania. North West J Zool. 2009;5: 170-8.
    Schaller GB. Wildlife of the Tibetan Steppe. Chicago: University of Chicago Press; 1998.
    Schaller GB. Tibet Wild. Washington: Island Press; 2012.
    Schaller GB, Junrang R, Mingjiang Q. Status of the snow Leopard Panthera uncia in Qinghai and Gansu Provinces, China. Biol Conserv. 1988;45: 179-94.
    Schoener TW. Competition and the form of habitat shift. Theor Popul Biol. 1974;6: 265-307.
    Shannon C, Weaver W. The mathematical theory of communication. Urbana: University of Illinois Press; 1949.
    Shehzad W, McCarthy TM, Pompanon F, Purevjav L, Coissac E, Riaz T, et al. Prey preference of snow leopard (Panthera uncia) in South Gobi, Mongolia. PLoS ONE. 2012;7: e32104.
    Shi ZY, Yang CQ, Hao MD, Wang XY, Ward RD, Zhang AB. FuzzyID2: a software package for large data set species identification via barcoding and metabarcoding using hidden Markov models and fuzzy set methods. Mol Ecol Resour. 2018;18: 666-75.
    Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am. 1994;87: 651-701.
    Simpson EH. Measurement of diversity. Nature. 1949;163: 688.
    Smith AT, Formozov NA, Hoffman RS, Zeng C, Erbajeva MA. The pikas. In: Chapman J, Flux J, editors. Rabbits, hares and pikas. Status survery and conservation action plan. Chapter 3. Gland, Switzerland: IUCN; 1990. pp. 14-60.
    Smith AT, Foggin JM. The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan plateau. Anim Conserv. 1999;2: 235-40.
    Soergel DAW, Dey N, Knight R, Brenner SE. Selection of primers for optimal taxonomic classification of environmental 16S rRNA gene sequences. ISME J. 2012;6: 1440-4.
    Symondson WOC. Molecular identification of prey in predator diets. Mol Ecol. 2002;11: 627-41.
    Taberlet P, Fumagalli L. Owl pellets as a source of DNA for genetic studies of small mammals. Mol Ecol. 1996;5: 301-5.
    Thiam M, Bâ K, Duplantier JM. Impacts of climatic changes on small mammal communities in the Sahel (West Africa) as evidenced by owl pellet analysis. African Zool. 2008;43: 135-43.
    Tremblay I, Thomas D, Blondel J, Perret P, Lambrechts MM. The effect of habitat quality on foraging patterns, provisioning rate and nestling growth in Corsican Blue Tits Parus caeruleus. Ibis. 2005;147: 17-24.
    Trevelline BK, Nuttle T, Porter BA, Brouwer N, Hoenig BD, Steffensmeier ZD, Latta SC. Stream acidification and reduced migratory prey availablity are associated with dietary shifts in an obligate riparian Neotropical migratory songbird. PeerJ. 2018a;16: e5141.
    Trevelline BK, Nuttle T, Hoenig BD, Brouwer NL, Porter BA, Latta SC. DNA metabarcoding of nestling feces reveals provisioning of aquatic prey and resource partitioning among Neotropical migratory songbirds in a riparian habitat. Oecologia. 2018b;187: 85-98.
    Treves A, Krofel M, McManus J. Predator control should not be a shot in the dark. Front Ecol Environ. 2016;14: 380-8.
    Valera F, Gutiérrez JE, Barrios R. Effectiveness, biases and mortality in the use of apomorphine for determining the diet of granivorous passerines. Condor. 1997;99: 765-72.
    Walter CB, O'Neill E. Electrophoresis in the study of diets and digestive rates of seabirds. Comp Biochem Physiol A Comp Physiol. 1986;84: 763-5.
    Wei WR, He JD, Zheng QY. Plateau pikas (Ochotona curzoniae) at low densities have no destructive effect on winter pasture in alpine meadows. Rangel J. 2020;42: 55-61.
    Wilson RP. An improved stomach pump for penguins and other seabirds. J Field Ornithol. 1984;55: 109-12.
    Xia W, Zhou X, Liu J, Zhang X. The bio-community in the region of alpine meadow. In: Liu J, Wang Z, editors. Alpine meadow ecosystem. Beijing, China: Science Press; 1991. p. 1-7.
    Yang Z, Gong M, Huang X, Li C, Liu X. Biodiversity of birds of prey in Shiqu county. J Sichuan Teach Coll. 2000;21: 137-40 (in Chinese).
    Zhang R, Ludwig A, Zhang C, Tong C, Li G, Tang Y, et al. Local adaptation of Gymnocypris przewalskii (Cyprinidae) on the Tibetan Plateau. Sci Rep. 2015;5: 9780.
    • Related Articles

  • Related Articles

    Jiangjian Xie, Zhulin Hao, Chunhe Hu, Changchun Zhang, Junguo Zhang. 2025: Beyond amplitude: Phase integration in bird vocalization recognition with MHAResNet. Avian Research, 16(1): 100229. DOI: 10.1016/j.avrs.2025.100229
    George Sangster, Kim Manzon Cancino, Robert O. Hutchinson. 2021: Taxonomic revision of the Savanna Nightjar (Caprimulgus affinis) complex based on vocalizations reveals three species. Avian Research, 12(1): 54. DOI: 10.1186/s40657-021-00288-z
    Jiaojiao Wang, Jianping Liu, Zhenqun Zhang, Hongxin Ren, Lijie Gao, Jianhua Hou. 2019: Is male condition corrected with song features in Dusky Warblers (Phylloscopus fuscatus). Avian Research, 10(1): 18. DOI: 10.1186/s40657-019-0158-5
    Heeyoung Kim, Jin-Won Lee, Jeong-Chil Yoo. 2017: Comparing vocal structures of the parasitic and nonparasitic groups in Cuculinae. Avian Research, 8(1): 27. DOI: 10.1186/s40657-017-0084-3
    Jiangping Yu, Weiwei Lv, Hongwei Xu, Nehafta Bibi, Yangyang Yu, Yunlei Jiang, Wei Liang, Haitao Wang. 2017: Function of note strings in Japanese Tit alarm calls to the Common Cuckoo: a playback experiment. Avian Research, 8(1): 22. DOI: 10.1186/s40657-017-0080-7
    Yang Li, Canwei Xia, Huw Lloyd, Donglai Li, Yanyun Zhang. 2017: Identification of vocal individuality in male cuckoos using different analytical techniques. Avian Research, 8(1): 21. DOI: 10.1186/s40657-017-0079-0
    Canwei Xia, Boye Liu, Daiping Wang, Huw Lloyd, Yanyun Zhang. 2015: Reliability of the Brownish-flanked Bush Warbler's soft song in male-male conflict. Avian Research, 6(1): 6. DOI: 10.1186/s40657-015-0015-0
    Johann H. VAN NIEKERK. 2013: Vocal structure, behavior and partitioning of all 23 Pternistis spp. into homologous sound (and monophyletic) groups. Avian Research, 4(3): 210-231. DOI: 10.5122/cbirds.2013.0020
    Jianqiang LI, Yanyun ZHANG, Zhengwang ZHANG. 2011: High frequency components in avian vocalizations. Avian Research, 2(3): 125-131. DOI: 10.5122/cbirds.2011.0019
    Jiliang XU, Zhengwang ZHANG. 2011: Home range and habitat composition of male Reeves's Pheasants in an agricultural-forest plantation landscape in central China: a preliminary report. Avian Research, 2(1): 53-58. DOI: 10.5122/cbirds.2011.0006

  • Cited by

    Periodical cited type(3)

    1. Justin Merondun, Cristiana I. Marques, Pedro Andrade, et al. Evolution and genetic architecture of sex-limited polymorphism in cuckoos. Science Advances, 2024, 10(17) DOI:10.1126/sciadv.adl5255
    2. Csaba Moskát, Márk E. Hauber. Syntax errors do not disrupt acoustic communication in the common cuckoo. Scientific Reports, 2022, 12(1) DOI:10.1038/s41598-022-05661-6
    3. Martina Esposito, Maria Ceraulo, Beniamino Tuliozi, et al. Decoupled Acoustic and Visual Components in the Multimodal Signals of the Common Cuckoo (Cuculus canorus). Frontiers in Ecology and Evolution, 2021, 9 DOI:10.3389/fevo.2021.725858

    Other cited types(0)

Catalog

    Figures(3)  /  Tables(1)

    Get Citation
    PDF
    XML

    Article Metrics

    Article has an altmetric score of 1
    Article has an altmetric score of 1
    Article views (577) PDF downloads (22) Cited by(3)
    Supported by: Beijing Renhe Information Technology Co. Ltd.   Technical support: info@rhhz.net

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return