Volume 13 Issue 1
Mar.  2022
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Article Contents
Abstract
1.   Introduction
2.   Methods
3.   Results
4.   Discussion
Authors' contribution
Ethics statement
Declaration of competing interest
Acknowledgements
References
Related Articles
Bin Wang, Yun Li, Guiquan Zhang, Jian Yang, Cao Deng, Haoyu Hu, Long Zhang, Xiaoqin Xu, Caiquan Zhou. 2022: Seasonal variations in the plant diet of the Chinese Monal revealed by fecal DNA metabarcoding analysis. Avian Research, 13(1): 100034. DOI: 10.1016/j.avrs.2022.100034
Citation: Bin Wang, Yun Li, Guiquan Zhang, Jian Yang, Cao Deng, Haoyu Hu, Long Zhang, Xiaoqin Xu, Caiquan Zhou. 2022: Seasonal variations in the plant diet of the Chinese Monal revealed by fecal DNA metabarcoding analysis. Avian Research, 13(1): 100034. DOI: 10.1016/j.avrs.2022.100034
shu

Seasonal variations in the plant diet of the Chinese Monal revealed by fecal DNA metabarcoding analysis

  • a.

    Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong, 637002, China

  • b.

    Institute of Ecology, China West Normal University, Nanchong, 637002, China

  • c.

    Key Laboratory of State Forestry and Grassland Administration on Conservation Biology of Rare Animals in the Giant Panda National Park (China Conservation and Research Center for the Giant Panda), Dujiangyan, 611830, China

  • d.

    Key Laboratory of Animal Disease and Human Health of Sichuan Province, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, 611130, China

  • e.

    Institute of Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, 100700, China

More Information
  • Corresponding author:

    E-mail address: wangbin513@cwnu.edu.cn (B. Wang)

    E-mail address: 310669804@qq.com (Y. Li)

    E-mail address: drcqzhou1@163.com (C. Zhou)

  • 1 These authors contributed equally to this work.

  • Received Date: 18 Oct 2021
  • Accepted Date: 24 Apr 2022
  • Available Online: 06 Jul 2022
  • Publish Date: 01 May 2022
    Graphical Abstract
    • Abstract

  • The Chinese Monal (Lophophorus lhuysii) is an alpine-obligate galliform species of global conservation priority. It has been listed as a first class protected wildlife species in China, requiring conservation actions during the 14th Five-Year Plan period. However, the diet composition of Chinese Monal and its seasonal variations have rarely been studied, constraining the effective conservation of the species. Here, we investigated the plant diet composition of the Chinese Monal and its seasonal variations using a DNA metabarcoding approach on fecal samples. We collected 190 fecal samples of the Chinese Monals from the central Qionglai Mountains located in China, and analyzed the plant diet of this species using a DNA metabarcoding approach. Taxonomic profiling of higher plants in the fecal samples was performed using the second internal transcribed spacer (ITS2) amplicon. Downstream analyses, including rarefaction curves, nonmetric multidimensional scaling (NMDS) and permutational multivariate analysis of variance (PERMANOVA), were used to explore the seasonal variations in diet composition. The Chinese Monal foraged a wide range of plant recipes composed of 35 families and 83 genera throughout the year, with Brassicaceae, Apiaceae, and Poaceae as the dominant families, and Cardamine as the dominant genus. The species consumed plants from 62 genera from 28 families during the breeding season (n ​= ​81) and 66 genera from 31 families during the non-breeding season (n ​= ​109). Further, the plant diet composition significantly varied between the breeding and non-breeding seasons, especially for the frequency of occurrence and relative read abundances at genus level. Our study analyzed the plant diet of the Chinese Monal at a high resolution for the first time, and the results revealed that the seasonal variations in its plant diet composition was adapted to plant phenology and foraging strategy. Fritillaria species, a previously confirmed important food resource for the Chinese Monal, were not detected in any fecal samples, potentially due to overharvesting of Fritillaria bulbs for Traditional Chinese Medicine. Therefore, we highly recommend further restriction of herb gathering in Chinese Monal habitats to facilitate the conservation of this endangered species. Altogether, our study enriches essential ecological information for the Chinese Monal and also provides insights into conservation management for this endangered species.

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  • Studies of animal behavior are conducted with the assistance of a variety of objects, including living animals (Ladu et al., 2015; Lawson et al., 2021) and non-living models comprising many different materials (Antunes and Biala, 2012; Lawson et al., 2021). These objects serve as stimuli in studies of the behavioral responses of animals within and across species, such as to conspecific intruders, potential mates, predators, and brood parasites. Non-living models, which may serve as replacements for systems involving living animals, are currently used frequently in animal behavior research, and they can be produced in a variety of ways. These models include the following: 1) taxidermy specimens from which the fur and/or feathers have been preserved, the body cavity stuffed with fillers such as cotton, and which have been preserved in antiseptic have been used by most studies, and include both stuffed models made by the researchers themselves and those borrowed from museums (Gill and Sealy, 1996; Schulze-Hagen et al., 2003; Welbergen and Davies, 2008; Henger and Hauber, 2014; Lawson et al., 2020); 2) sculptural models, which are produced by craftspeople from wood or plastic and then painted in the appropriate colors (Welbergen and Davies, 2012; Thorogood and Davies, 2016); 3) freeze-dried models, which are the direct sublimation of the solvent from the frozen animal's body at ultra-low temperatures, and are more durable than taxidermy specimens and maintain a relatively lifelike appearance (Bazin and Sealy, 1993; Maizato et al., 2013; Shoffner and Brittingham, 2013); and 4) three-dimensional (3D) printed models produced using 3D-printing technology, which have developed rapidly in recent years because of their repeatable, precise, and standardized production qualities (Conner et al., 2014; Behm et al., 2018). Inevitably, 3D-printed models also have certain limitations: they are static, and thus unable to simulate living organisms; only small objects can be printed; and their materials they are made of may contain toxic chemicals or be difficult to degrade. However, these deficiencies can be addressed by installing robots inside the models, assembling multiple printed parts into a larger model, and using recyclable materials (Walker and Humphries, 2019).

    Although 3D-printing technology has been widely used in some aspects of behavioral studies, it is rarely used in avian brood parasitism (ABP), especially for studies of behavioral reaction to nest intruders (but see Chaumont et al., 2021), not to mention being recognized as a standard methodology in this research domain. However, using models as research tools is important in studies of ABP. Because the parasitism includes a series of steps from approaching a host nest (Feeney et al., 2012) to laying a parasite egg (Peer and Sealy, 1999; Soler, 2014) and manipulating the host parent (Soler et al., 1995, 1999; Swan et al., 2015), testing the host response against the parasite and its egg is a key to understand the coevolutionary interaction between the host and parasite. For example, to test the recognition on parasite egg by the host, model eggs that simulate the parasite eggs were widely used for artificial parasitism. The standard method for this experiment was to use hand-made model eggs made of polymer clay (Antonov et al., 2009; Yi et al., 2020; Yang et al., 2022a, b). Hitherto, only few studies have used 3D-printed model eggs for artificial parasitism (Igic et al., 2015; Dainson et al., 2017; Hays and Hauber, 2018; Abolins-Abols et al., 2019; Yang et al., 2019; Butler et al., 2020; Luro et al., 2020; Hauber et al., 2021). Furthermore, to test the host response toward parasite approaching its nest for parasitism, researchers generally used taxidermy specimen as a standard method (Gill and Sealy, 1996; Welbergen and Davies, 2008; Henger and Hauber, 2014; Lawson et al., 2020; Yang et al., 2022a, b), while using 3D-printed animal model was rare and its feasibility has not been evaluated. For example, Chaumont et al. (2021) used 3D-printed cuckoo models for ABP studies, but they did not make a comprehensive comparison and evaluation between 3D-printed models and taxidermy specimens. The purpose of this study is to provide an applied example of the use of 3D-printed models that simulate avian predators and brood parasites to test the behavioral reaction of a widespread bird species, the Oriental Reed Warbler (Acrocephalus orientalis), and also to evaluate the feasibility and advantages of using 3D-printed animal models for studies of animal behavior. We also provide some suggestions for future studies on ABP with 3D-printed animal models.

    2.1   Study area and species

    We performed this study in Yongnianwa National Wetland Park (36°40ʹ–36°41ʹ N, 114°41ʹ–114°45ʹ E) during the breeding season (May–July) of the Oriental Reed Warbler (hereafter the Reed Warbler) in 2021. The study site is a wetland habitat in a temperate semi-humid continental monsoon climate in Hebei Province in China, with the Common Reed (Phragmites australis) being the major herbaceous plant. The annual average temperature is 12.9 ​℃, and the annual average precipitation totals 527.8 ​mm (Wang and Yang, 2020). The Reed Warbler belongs to the family Acrocephalidae, Passeriformes (Zheng, 2017), and is one of the main hosts of the Common Cuckoo (Cuculus canorus) in the study area; previous studies have found a parasitic rate of 14.8% in this study population (Ma et al., 2018; Wang et al., 2021).

    2.2   3D-printed animal models

    We used three types of 3D-printed animal models, one each of the Sparrowhawk (Accipiter nisus), Common Cuckoo, and Oriental Turtle Dove (Streptopelia orientalis). These were designed using 3D Studio Max 2015 for Windows (Autodesk Inc., California, USA) and printed on a Digital Light Processing (DLP) 3D printer (StarRAY SP-DD230, Sprintray Inc., Guangdong, China). The models were then painted according to the natural phenotype of the animals (Fig. 1). These species are all sympatric with the Reed Warbler. The Sparrowhawk is a predator that preys on adult Reed Warblers (Wang et al., 2021) and the Common Cuckoo (hereafter the Cuckoo) is a brood parasite and nest predator that can threaten the nest, but not the adult Reed Warbler (Yang et al., 2017). The Oriental Turtle Dove (hereafter the Dove) is harmless to the Reed Warbler and here served as a control.

    Figure  1.  The 3D-printed animal models used for testing the behavioral response of the Oriental Reed Warbler: (A) Sparrowhawk; (B) Common Cuckoo; (C) Oriental Turtle Dove.
    DownLoad: Full-Size Img PowerPoint

    2.3   Field experiment

    In the experiment, each Reed Warbler nest during the early incubation stage (the first three days of incubation) received the three animal models above as stimuli, with 1-h intervals between every two models. Each model was randomly selected and placed at a distance of 0.5 ​m in front of a nest, at the same height as the nest. We recorded the reaction from the Reed Warbler over the next 5 ​min with a digital video recorder (DMC-TS30, Panasonic Corporation, Xiamen, China), dividing actions into attacking (score ​= ​4), mobbing (score ​= ​3), alarm calling (score ​= ​2), and no reaction (score ​= ​1). We recorded the strongest level of reaction (a higher score refers to a stronger level) if a Reed Warbler presented more than one reaction during the experiment. A result of no reaction refers to the Reed Warbler ignoring the decoy. To evaluate the use of 3D-printed animal models, we conducted another experiment with the same procedure except the animal models were replaced with taxidermy specimens, these being a classical method for testing the behavioral reactions of animals. To avoid pseudoreplication, two replicates of 3D-printed animal models or taxidermy specimens were randomly selected for the experiment. The Reed Warbler is sexually monomorphic, so we did not distinguish different individuals by sex during experiments.

    2.4   Statistical analyses

    A cumulative link mixed model (CLMM) was used to analyze the reaction of Reed Warbler toward different types of stimuli. In this experiment the reaction (score 1–4) was the response; the trial (3D-printed animal model vs. taxidermy specimens), stimuli (Sparrowhawk, Cuckoo, or Dove), and replicate (two per model or specimen) were included as the fixed effects; and the clutch size, egg-laying date (of first egg), and nest identity were used as the random effects. The interactions between trial and stimuli and between trial and replicate were also tested. A post-hoc test using the Tukey method for P-value adjustment was used for pairwise comparison between different stimuli according to the trial.

    2.5   Prediction and evaluation

    The Dove is harmless to the Reed Warbler, so it was used here as a reference for reaction comparison. We predicted that the Dove would elicit the least intense reaction out of the three stimuli. The Cuckoo is a brood parasite and predator to the nest, and while it can have a highly negative impact on the reproductive success of the Reed Warbler, it is not dangerous to the adult birds themselves. The Sparrowhawk is a bird of prey, threatening adult Reed Warblers. Therefore, we predicted that the warblers would react more strongly to the Cuckoo than to the Sparrowhawk, because the former should trigger a mobbing and attacking reaction that is effective against the Cuckoo but dangerous when used on the Sparrowhawk. Furthermore, we predicted that the Reed Warbler would react consistently to the specimens and 3D-printed models if the latter was feasible as a substitution for the former.

    The reaction scores for the Dove, Cuckoo, and Sparrowhawk taxidermy specimens were 1.467 ​± ​0.516, 3.333 ​± ​0.816, and 2.267 ​± ​0.799, respectively (n ​= ​15 for all). For the 3D-printed animal models, these values were 1.467 ​± ​0.516, 3.400 ​± ​0.632, and 2.133 ​± ​0.640 (n ​= ​15 for all). As we predicted, the reaction intensity followed a gradient from Dove (lowest) to Sparrowhawk (medium) to Cuckoo (highest). CLMM analyses showed that neither the trial (Z ​= ​0.228, P ​= ​0.819) nor the replicate (Z ​= ​0.134, P ​= ​0.893) had any significant differences. However, the Reed Warbler's reactions to stimuli did differ significantly between Dove and Cuckoo (Z ​= ​5.495, P ​ < ​0.001, CLMM) and between Dove and Sparrowhawk (Z ​= ​3.841, P ​ < ​0.001, CLMM). No statistically significant differences were observed in the interaction between trial and stimuli, nor between the trial and replicate (Table 1). Pairwise comparison indicated significant differences between the reactions of the Reed Warbler to the Cuckoo and to the Sparrowhawk for both specimens (t ​= ​4.398, P ​ < ​0.001, Post-hoc test) and 3D-printed models (t ​= ​5.222, P ​ < ​0.001, Post-hoc test; Table 2).

    Table  1.  Reaction of Oriental Reed Warbler to different stimuli by using cumulative link mixed model.
    Fixed effect Reference variable Compared variable Estimate SE Z P
    Trial Specimen 3D model 0.134 0.585 0.228 0.819
    Stimuli Dove Cuckoo 3.816 0.694 5.495 < 0.001
    Sparrowhawk 1.876 0.539 3.841 < 0.001
    Replicate Replicate 1 Replicate 2 0.053 0.398 0.134 0.893
    Trial × Stimuli Specimen × Dove 3D model × Cuckoo 0.110 0.646 0.169 0.865
    3D model × Sparrowhawk −0.217 0.645 −0.336 0.737
    Trial × replicate Specimen × Replicate 1 Model × Replicate 2 −0.301 0.574 −0.524 0.600
    Random effect: clutch size, egg-laying date, and nest identity.
     | Show Table
    DownLoad: CSV
    Table  2.  Results of pairwise comparison between stimuli for specimens and models using Tukey method.
    Empty Cell Estimate SE df t P
    Taxidermy specimens
    Cuckoo vs. Dove 1.867 0.243 84 7.696 < 0.001
    Cuckoo vs. Sparrowhawk 1.067 0.243 84 4.398 < 0.001
    Dove vs. Sparrowhawk −0.800 0.243 84 −3.298 0.004
    3D-printed models
    Cuckoo vs. Dove 1.933 0.243 84 7.97 < 0.001
    Cuckoo vs. Sparrowhawk 1.267 0.243 84 5.222 < 0.001
    Dove vs. Sparrowhawk −0.667 0.243 84 −2.748 0.019
     | Show Table
    DownLoad: CSV

    Our results indicated that the Reed Warbler was reacting to the taxidermy specimens and 3D-printed animal models consistently. This study thus supports the conclusion that the use of 3D-printed animal models to substitute specimens is a feasible means of testing animal behavior. We suggest that the use of 3D-printed animal models should be extended as a standard method for studies of host nest defense in ABP because of their clear advantages: (1) High sustainability: compared to living animals or taxidermy specimens, 3D-printed models are more sustainable in utilization because they are beneficial for the biological conservation. The taxidermy specimens need strict storage conditions and are easily damaged (e.g., destroyed by the host) during experiments (Davies and Brooke, 1988; Welbergen and Davies, 2008, 2012), which undoubtedly leads to a need for constant supplement. Such a requirement for specimens would involve commercial interests, which may have a negative effect on the natural animal population, especially in developing and underdeveloped countries. (2) High comparability: using 3D-printed models would increase the comparability between different studies because their postures can be controlled and standardized, allowing for specific criteria to be shared between different studies. For example, researchers around the world can share their 3D model documents through scientific references. By contrast, both the posture and color may vary across different studies that use animal specimens or handcrafted models because they differ between manufacturers and crafters. It is impossible to make highly consistent specimens or handcrafted models, even from the same craftsperson. (3) High controllability: for the 3D-printed models, it is easy to manipulate one of the characteristics while controlling for others, which allows us to test the animal response to a specific trait or a combination of some traits optionally and independently. This idea has been proposed for the use of 3D-printed model eggs, which allows the researchers to change the characteristics of model eggs in one dimension while controlling for others (Yang et al., 2019). For the animal models, they have more characteristics and are more complicated, which makes such controllability more significant. For example, to test the size effect of nest intruders on host response, we can simply manipulate the size of the animal models while keeping all the other traits consistent. Yu et al. (2020) tested such size effects on a host, but the taxidermy specimens they used differed across many other traits because the specimens were different parasite species. It is not possible to change some characteristics of the taxidermy specimens while controlling for others, but this is easy for 3D-printed animal models.

    In summary, this study provides supportive evidence that 3D-printed animal models can be used as a standard method for studies of ABP. The use of 3D-printed animal models brings a series of advantages, which are beneficial for biological conservation and make research studies more comparable and controllable. We believe this standard method allows the researchers to collect more objective and scientific data, which could reveal the visual signal cues of host recognition in more detail and thus help us better understand the coevolution between brood parasites and hosts in ABP studies.

    CY designed the study, and YC and CY carried out laboratory and statistical analyses. XC and JW performed field experiments. XC and CY wrote the draft manuscript, and CY improved the manuscript. All authors read and approved the final manuscript.

    The experiments comply with the current laws of China. Fieldwork was carried out under the permission from the Yongniwa National Natural Park.

    The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

    This study was supported by the Education Department of Hainan Province (HnjgY2022-12), Hainan Provincial Natural Science Foundation of China (320CXTD437 and 2019RC189), the National Natural Science Foundation of China (32260127 and 31672303) to CY, and the Hainan Provincial Innovative Research Program for Graduates (Qhyb2021-55) to XC.

    • References (58)
  • Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32-46.
    Ando, H., Fujii, C., Kawanabe, M., Ao, Y., Inoue, T., Takenaka, A., 2018. Evaluation of plant contamination in metabarcoding diet analysis of a herbivore. Sci. Rep. 8, 15563.
    Birdlife International, 2016. Lophophorus lhuysii. The IUCN Red List of Threatened Species 2016: e. T22679192A92806697. . (Accessed 04 September 2020).
    Callahan, B.J., Mcmurdie, P.J., Holmes, S.P., 2017. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 11, 2639-2643.
    Chen, D., Li, C., Feng, L., Zhang, Z., Zhang, H., Cheng, G., et al., 2018. Analysis of the influence of living environment and age on vaginal fungal microbiome in giant pandas (Ailuropoda melanoleuca) by high throughput sequencing. Microb. Pathogen. 115, 280-286.
    Chen, Y.H., 2013. Conservation priority for endemic birds of mainland China based on a phylogenetic framework. Chinese Birds 4, 248-253.
    Chua, P.Y.S., Lammers, Y., Menoni, E., Ekrem, T., Bohmann, K., Boessenkool, S., et al., 2021. Molecular dietary analyses of western capercaillies (Tetrao urogallus) reveal a diverse diet. Environ. DNA 3, 1156-1171.
    Chung, C.T., Wong, H.S., Kwok, M.L., Meng, Q., Chan, K.M., 2021. Dietary analysis of the House Swift (Apus nipalensis) in Hong Kong using prey DNA in faecal samples. Avian Res. 12, 5.
    CITES, 2016. Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendices I, II and III. . (Accessed 04 September 2020).
    Deagle, B.E., Thomas, A.C., McInnes, J.C., Clarke, L.J., Vesterinen, E.J., Clare, E.L., et al., 2019. Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data? Mol. Ecol. 28, 391-406.
    Fahner, N.A., Shokralla, S., Baird, D.J., Hajibabaei, M., 2016. Large-scale monitoring of plants through environmental DNA metabarcoding of soil: recovery, resolution, and annotation of four DNA markers. PLoS ONE 11, e0157505.
    Forin-Wiart, M-A., Poulle, M-L., Piry, S., Cosson, J-F., Larose, C., Galan, M., 2018. Evaluating metabarcoding to analyse diet composition of species foraging in anthropogenic landscapes using Ion Torrent and Illumina sequencing. Sci. Rep. 8, 17091.
    Gainsbury, A., Meiri, S., 2017. The latitudinal diversity gradient and interspecific competition: no global relationship between lizard dietary niche breadth and species richness. Global Ecol. Biogeogr. 26, 563-572.
    Gao, Z.T., Wang, X.Y., Liu, Y., Wei, X.M., Han, J.P., Chen, S.L., 2018. Identification of Chinese patent medicines containing Fritillariae cirrhosae bulbus using ITS2 region. Sci. Sin. Vitae 48, 482-489. (in Chinese).
    Gotelli, N.J., Colwell, R.K., 2011. Estimating species richness. In: Magurran, A.E., McGill, B.J. (Eds.), Frontiers in Measuring Biodiversity. Oxford University Press, New York, pp. 39-54.
    Gul, M.R., Griffen, B.D., 2020. Diet, energy storage, and reproductive condition in a bioindicator species across beaches with different levels of human disturbance. Ecol. Indic. 117, 106636.
    Guo, L., Liu, F.Q., Shi, L., Wen, L.Y., 2020. Physiological and ecological adaptability of Blood Pheasant (Ithaginis cruentus) and its favorite Bryophyte. Chin. J. Appl. Environ. Biol. 26, 1400-1405. (in Chinese).
    Hacker, C.E., Hoenig, B.D., Wu, L., Cong, W., Yu, J., Dai, Y., et al., 2021. Use of DNA metabarcoding of bird pellets in understanding raptor diet on the Qinghai-Tibetan Plateau of China. Avian Res. 12, 42.
    He, F.Q., Lu, T.C., 1985. Ecology of the Chinese Monal in winter. Zool. Res. 6, 345-352. (in Chinese).
    He, F.Q., Lu, T.C., Lu, C.L., Cui, X.Z., 1986. Study on the breeding ecology of the Chinese Monal. Acta Ecol. Sin. 6, 186-192. (in Chinese).
    Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Method. Ecol. Evol. 7, 1451-1456.
    IUCN, 2020. The IUCN red list of threatened species. Version 2020-2. . (Accessed 04 September 2020).
    Jayawardena, R.S., Purahong, W., Zhang, W., Wubet, T., Li, X., Liu, M., et al., 2018. Biodiversity of fungi on Vitis vinifera L. revealed by traditional and high-resolution culture-independent approaches. Fungal Divers. 90, 1-84.
    Jia, H.Y., Liu, X.Q., Tian, N.F., Zhang, R., Wang, R.R., Liu, L.X., et al., 2021. Spring and summer diet composition of Tibetan Snowcocks. Chinese J. Ecol. 40, 470-479. (in Chinese).
    Kartzinel, T.R., Chen, P.A., Coverdale, T.C., Erickson, D.L., Kress, W.J., Kuzmina, M.L., et al., 2015. DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc. Nat. Acad. Sci. 112, 8019-8024.
    Kluen, E., Nousiainen, R., Lehikoinen, A., 2017. Breeding phenological response to spring weather conditions in common Finnish birds: resident species respond stronger than migratory species. J. Avian Biol. 48, 611-619.
    Long, T.L., Shao, K., Guo, G., Cheng, C.Y., Zou, X.Y., Landel, H., et al., 1998. Field tracking and ecological observation of the Chinese Monal in winter. Sichuan J. Zool. 17, 104-105. (in Chinese).
    Lu, T.C., Liu, R.S., He, F.Q., Lu, C.L., 1986. Ecological studies on Chinese Monal. Acta Zool. Sin. 32, 273-279. (in Chinese).
    Luo, K., Ma, P., Yao, H., Song, J., Chen, K., Liu, Y., 2012a. Molecular identification of Fritillariae cirrhosae Bulbus and its adulterants. World Sci. Technol. Modern. Tradit. Chin. Med. Materia Medica 14, 1153-1158. (in Chinese).
    Luo, X., Wu, T.P., Huang, A.Q., 2016. Diet analysis and foraging strategy of two sympatric pheasants at Mt. Gaoligong in winter. Chin. J. Ecol. 35, 1003-1008. (in Chinese).
    Luo, X., Xu, M.Y., Wu, L.X., 2012b. Spring diets and food nutrients of Sclater's Monal at Mt. Gaoligong, China. Sichuan J. Zool. 31, 17-22. (in Chinese).
    Ma, G.Y., 1988. Observation on the Chinese Monal in Gansu Province. Sichuan J. Zool. 7, 41-42. (in Chinese).
    Martin, K., Hik, D., 1992. Willow Ptarmigan chicks consume moss sporophyte capsules. J. Field Ornithol. 63, 355-358.
    McClenaghan, B., Nol, E., Kerr, K.C.R., 2019. DNA metabarcoding reveals the broad and flexible diet of a declining aerial insectivore. Auk 136, 1-11.
    McInnes, J.C., Alderman, R., Deagle, B.E., Lea, M-A., Raymond, B., Jarman, S.N., 2017. Optimised scat collection protocols for dietary DNA metabarcoding in vertebrates. Method. Ecol. Evol. 8, 192-202.
    Moorhouse-Gann, R.J., Dunn, J.C., De Vere, N., Goder, M., Cole, N., Hipperson, H., et al., 2018. New universal ITS2 primers for high-resolution herbivory analyses using DNA metabarcoding in both tropical and temperate zones. Sci. Rep. 8, 8542.
    National Forestry and Grassland Administration, National Development and Reform Commission, 2021. The outline of the national 14th Five-Year Plan on development of forestry and grassland conservation. . (in Chinese).
    Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., Mcglinn, D., et al., 2020. vegan: community ecology package. R package version 2.5-7. .
    Pompanon, F., Deagle, B.E., Symondson, W.O.C., Brown, D.S., Jarman, S.N., Taberlet, P., 2012. Who is eating what: diet assessment using next generation sequencing. Mol. Ecol. 21, 1931-1950.
    Prins, H.H.T., 1982. Why are mosses eaten in cold environments only? Oikos 38, 374-380.
    R Core Team, 2021. R: a language and environment for statistical computing. .
    Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahe, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584.
    Shao, X.N., Lu, Q., Xiong, M.Y., Bu, H.L., Shi, X.Y., Wang, D.J., et al., 2021. Prey partitioning and livestock consumption in the world's richest large carnivore assemblage. Curr. Biol. 31, 4887-4897.
    Shutt, J.D., Trivedi, U.H., Nicholls, J.A., 2021. Faecal metabarcoding reveals pervasive long-distance impacts of garden bird feeding. Proc. R. Soc. B. Biol. 288, 20210480.
    Teng, L.W., Li, Y.X., Liu, Z.S., Dong, J.P., Yao, Z.C., Zhang, J.T., 2013. Summer diet composition of feral yak in Helan Mountains. J. Econ. Anim. 17, 192-196. (in Chinese).
    Teng, L.W., Wang, Y., Li, L.Y., Yao, Z.C., Lu, P.F., Li, Y.X., et al., 2014. Autumn diet composition of feral yak (Bos grunnieus) in Helan Mountains. J. Anhui Agr. Sci. 42, 6258-6260. (in Chinese).
    Wang, B., Xu, Y., Ran, J.H., 2017. Predicting suitable habitat of the Chinese Monal (Lophophorus lhuysii) using ecological niche modeling in the Qionglai Mountains, China. PeerJ 5, e3477.
    Ward, E.J., Levin, P.S., Lance, M.M., Jeffries, S.J., Acevedogutierrez, A., 2012. Integrating diet and movement data to identify hot spots of predation risk and areas of conservation concern for endangered species. Conserv. Lett. 5, 37-47.
    Wickham, H., 2009. ggplot2: elegant graphics for data analysis. Springer-Verlag, New York.
    Xu, L.X., Wu, W., Ma, S.G., Ma, J., Cheng, K., 2015. Winter food habits of Hazal Grouse (Bonasa bonasia) in Liangshui National Nature Reserve. Chinese J. Wildl. 36, 402-406. (in Chinese).
    Xu, Y., Wang, B., Zhong, X., Yang, B., Zhang, J.D., Zhao, C., et al., 2020. Predicting range shifts of the Chinese Monal (Lophophorus lhuysii) under climate change: Implications for long-term conservation. Global Ecol. Conserv. 22, e01018.
    Yao, Z.C., Liu, Z.S., Wang, Z.D., Hu, T.H., Li, Z.G., 2011. Winter and spring diet composition of feral yak in Helan Mountains, China. Acta Ecol. Sin. 31, 673-679. (in Chinese).
    Yu, X., Chen, J.C., Wang, B., Yan, Y., Ran, J.H., He, F., et al., 2017. Population density estimation and habitat suitability assessment of Lophophorus lhuysii during breeding season in Xiaozhaizigou National Nature Reserve, Sichuan Province. Sichuan J. Zool. 36, 361-367. (in Chinese).
    Zhang, B.W., Li, M., Ma, L.C., Wei, F.W., 2006. A widely applicable protocol for DNA isolation from fecal samples. Biochem. Genet. 44, 503-512.
    Zhang, T., 1995. Distribution and ecology of Chinese Monals in Baishuijiang Nature Reserve, Gansu. Chinese J. Zool. 30, 25-28. (in Chinese).
    Zhang, Z.W., Ding, C., Ding, P., Zheng, G., 2003. The current status and a conservation strategy for species of Galliformes in China. Biodivers. Sci. 11, 414-421.
    Zheng, G.M., 2015. Pheasants in China. Higher Education Press, Beijing.
    Zheng, H., Deng, K.Y., Chen, A.Q., Fu, S.B., Zhou, D., Wang, W.W., et al., 2019. Molecular identification and genetic relationship of Fritillaria cirrhosa and related species based on DNA barcode. Acta Pharm. Sin. 54, 2326-2334. (in Chinese).
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