Dietary composition and seasonal changes of the Tibetan fox (Vulpes ferrilata)

doi:10.16829/j.slxb.150794

Abstract

Abstract: The Tibetan fox (Vulpes ferrilata) is a crucial predator in the food chain in the stepper area of the Tibetan Plateau. Studies about its diet have important theoretical significance to understand its relationships with prey species, ecological adaptation strategies, and the transmission mechanism of parasitic zoonosis mediated by the food chain. In this study, 30 and 28 fecal samples of Tibetan foxes were collected from Shiqu County, Sichuan Province, during the warm season (July and August) and cold season (November) in 2019, respectively. Meta-barcode sequencing and microscopic observation were performed to analyze the dietary composition of the Tibetan fox and its seasonal differences. Results showed that the Tibetan fox mainly fed on pikas, rodents, birds, ungulates, fishes, and also insects and plants. Pikas represented by the plateau pika (Ochotona curzoniae) and the Phasianidae birds had the highest detection rates in the feces of the Tibetan fox, representing thus its main prey. Their detected rates in fecal samples did not change significantly between the cold and warm seasons. The Chi-square test showed that the frequency of Procypris (Cypriniformes: Cyprinidae) and insects in the fecal samples of Tibetan foxes in the warm season were significantly higher than that in the cold season. The α diversity and evenness of food composition in the feces of Tibetan foxes in the cold season were higher than that in the warm season, but there was no significant difference. Linear discriminant analysis effect size revealed that DNA reads of Procypris spp. in the fecal samples of the Tibetan fox in the warm season were significantly higher than that in the cold season. The principal coordinate analysis showed that food items and their sequence abundance in various fecal samples of warm season were more similar than those in samples of cold season. These results indicated that Tibetan foxes tend to prey on prevailing prey species in the warm season when food resources are more abundant, while in the the cold season, when prey resources are relatively scarcer, they increase the width of feeding niche to obtain more edible food items. This study provided fundamental information about the feeding ecology of the Tibetan fox, and its significance in the conservation and prevention of zoonotic diseases transmitted along the food chain was discussed.

Key words: Tibetan fox, Dietary analysis, Seasonal variation, Non-invasive sampling, Metabarcoding

摘要： 作为青藏高原地区食物链高端的捕食者，藏狐(Vulpes ferrilata)的食物组成研究不仅有助于了解该物种与当地潜在被捕食物种之间的种间关系，同时对于了解其生态适应策略及捕食食物链介导的野生动物疫源疫病的传播机制具有重要理论意义。本研究对2019年暖季(7—8月)和寒季(11月)分别在四川省甘孜州石渠县采集的30份和28份藏狐粪便样品，进行DNA宏条形码测序和显微观察，分析藏狐的食物组成及其季节差异。结果显示，藏狐主要取食包括啮齿类、鸟类、有蹄类、鱼类在内的多种脊椎动物以及昆虫和植物。以高原鼠兔(Ochotona curzoniae)为代表的鼠兔科动物和雉科鸟类是藏狐最主要的食物来源，在藏狐粪便中检出率最高，且在寒季和暖季之间没有显著差异。卡方检验显示鲤形目鲤科原鲤属鱼类(Procypris spp.)和昆虫在暖季藏狐粪便中出现频次显著高于寒季。寒季藏狐粪便中食物组成的α多样性和均匀度均高于暖季，但无显著差异。线性判别分析发现原鲤属鱼类在暖季藏狐粪便中的序列丰度显著高于寒季。主坐标分析显示暖季粪便内不同食物类型和序列丰度更加相似，而寒季粪便内不同食物类型和序列丰度具有更大差异。这些结果揭示：当暖季食物资源丰富度较高时，藏狐倾向于捕食丰富度较高的猎物物种，而当寒季各类猎物资源相对匮乏时，藏狐则通过增加取食生态位宽度以尽可能获取可以食用的食物来适应寒季更为严酷的生存环境。本研究在丰富藏狐食性资料的同时，为野生动物保护及沿食物链传播的人兽共患病的防治工作提供基础数据。

关键词: 藏狐, 食性分析, 季节性差异, 非损伤性取样, DNA宏条形码技术

CLC Number:

Q958. 12

ZHENG Jiaxin, ZUO Qingqiu, WANG Gang, WEI Xu, WENG Xiaodong, WANG Zhenghuan. Dietary composition and seasonal changes of the Tibetan fox (Vulpes ferrilata)[J]. ACTA THERIOLOGICA SINICA, 2023, 43(4): 398-411.

郑佳鑫, 左清秋, 王刚, 韦旭, 翁晓东, 王正寰. 藏狐的食物组成及其季节差异[J]. 兽类学报, 2023, 43(4): 398-411.

References

Andriollo T, Michaux J R, Ruedi M. 2021. Food for everyone:differential feeding habits of cryptic bat species inferred from DNA metabarcoding. Molecular Ecology, 30 (18):4584-4600.
Arthur A D, Pech R P, Jiebu, Zhang Y M, Lin H. 2007. Grassland degradation on the Tibetan Plateau:the role of small mammals and methods of control. Canberra:The Australian Centre for International Agricultural Research, 11.
Bolyen E, Rideout J R, Dillon M R, Bokulich N A, Abnet C C, AlGhalith G A, Alexander H, Alm E J, Arumugam M, Asnicar F, Bai Y, Bisanz J E, Bittinger K, Brejnrod A, Brislawn C J, Brown C T, Callahan B J, Caraballo-Rodríguez A M, Chase J, Cope E K, Silva R D, Diener C, Dorrestein P C, Douglas G M, Durall D M, Duvallet C, Edwardson C F, Ernst M, Estaki M, Fouquier J, Gauglitz J M, Gibbons S M, Gibson D L, Gonzalez A, Gorlick K, Guo J R, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley G A, Janssen S, Jarmusch A K, Jiang L J, Kaehler B D, Kang K B, Keefe C R, Keim P, Kelley S T, Knights D, Koester I, Kosciolek T, Kreps J, Langille M G I, Lee J, Ley R, Liu Y X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin B D, Mcdonald D, Mciver L J, Melnik A V, Metcalf J L, Morgan S C, Morton J T, Naimey A T, Navas-Molina J A, Nothias L F, Orchanian S B, Pearson T, Peoples S L, Petras D, Preuss M L, Pruesse E, Rasmussen L B, Rivers A, Robeson M S N, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song S J, Spear J R, Swafford A D, Thompson L R, Torres P J, Trinh P, Tripathi A, Turnbaugh P J, Ul-Hasan S, Hooft J J J V, Vargas F, Vázquez-Baeza Y, Vogtmann E, Hippel M V, Walters W, Wan Y H, Wang M X, Warren J, Weber K C, Williamson C H D, Willis A D, Xu Z Z, Zaneveld J R, Zhang Y L, Zhu Q Y, Knight R, Caporaso J G. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37 (8):852-857.
Braczkowski A R, O'Bryan C J, Stringer M J, Watson J E, Possingham H P, Beyer H L. 2018. Leopards provide public health benefits in Mumbai, India. Frontiers in Ecology and the Environment, 16(3):176-182.
Calvignac-Spencer S, Merkel K, Kutzner N, Kühl H, Boesch C, Kappeler P M, Metzger S, Schubert G, Leendertz F H. 2013. Carrion fly-derived DNA as a tool for comprehensive and cost-effective assessment of mammalian biodiversity. Molecular Ecology, 22(4):915-924.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T L. 2009. BLAST+:architecture and applications.Bmc Bioinformatics, 10 (12):421.
Chattopadhyay J, Arino O. 1999. A predator-prey model with disease in the prey. Nonlinear Analysis:Theory, Methods & Applications, 36 (6):747-766.
Chetri M, Odden M, Wegge P. 2017. Snow leopard and Himalayan wolf:food habits and prey selection in the central Himalayas, Nepal. PLoS ONE, 12 (2):e170549.
Ciucci P, Tosoni E, Di Domenico G, Quattrociocchi F, Boitani L. 2014. Seasonal and annual variation in the food habits of Apennine brown bears, central Italy. Journal of Mammalogy, 95 (3):572-586.
Clark H O, Newman D P, Murdoch J D, Tseng J, Wang Z H, Harris R B. 2008. Vulpes ferrilata (Carnivora:Canidae). Mammalian Species, 40 (821):1-6.
Cristescu M E. 2014. From barcoding single individuals to metabarcoding biological communities:towards an integrative approach to the study of global biodiversity. Trends in Ecology & Evolution, 29 (10):566-571.
De Barba M, Miquel C, Boyer F, Mercier C, Rioux D, Coissac E, Taberlet P. 2014. DNA metabarcoding multiplexing and validation of data accuracy for diet assessment:application to omnivorous diet. Molecular Ecology Resources, 14 (2):306-323.
Davidson Z, Valeix M, Van Kesteren F, Loveridge A J, Hunt J E, Murindagomo F, Macdonald D W. 2013. Seasonal diet and prey preference of the African lion in a waterhole-driven semiarid savanna. PLoS ONE, 8 (2):e55182.
Feng Z J, Cai G Q, Zheng C L. 1986. The Mammals of Xizang. Beijing:Science Press, 132-134. (in Chinese)
Figueiredo A M, Valente A M, Barros T, Carvalho J, Silva D A, Fonseca C, Carvalho L M D, Torres R T. 2020. What does the wolf eat? Assessing the diet of the endangered Iberian wolf (Canis lupus signatus) in northeast Portugal. PLoS ONE, 15 (3):e230433.
Fiore A D. 2004. Diet and feeding ecology of woolly monkeys in a western Amazonian Rain Forest. International Journal of Primatology, 25 (4):767-801.
Gong L X, Gu H, Chang Y, Wang Z Q, Biye S, Lin A Q, Hui W, Feng J, Jiang T L. 2023. Seasonal variation of population and individual dietary niche in the avivorous bat, Ia io. Oecologia, 201(3):1-15.
Harris R B, Zhou J K, Ji Y Q, Zhang K, Yang C Y, Yu D W. 2014. Evidence that the Tibetan fox is an obligate predator of the plateau pika:Conservation implications. Journal of Mammalogy, 95 (6):1207-1221.
Ingerson-Mahar J. 2002. Relating diet and morphology in adult Carabid beetles. In:Holland J M ed. The Agroecology of Carabid Beetles. Andover:Intercept Limited, 111-136.
Jȩdrzejewski W, Jȩdrzejewska B, Okarma H, Schmidt K, Zub K, Musiani M. 2000. Prey selection and predation by wolves in BiaŁowieŻa Primeval Forest, Poland. Journal of Mammalogy, 81(1):197-212.
Ji Y Q, Baker C C M, Popescu V D, Wang J X, Wu C Y, Wang Z Y, Li Y H, Wang L, Hua C L, Yang Z X, Yang C Y, Xu C C Y, Diana A, Wen Q, Pierce N E, Yu D W. 2022. Measuring protected-area effectiveness using vertebrate distributions from leech iDNA. Nature Communications, 13 (1):1555.
Kocher T D, Thomas W K, Meyer A, Edwards S V, Paabo S, Villablanca F X, Wilson A C. 1989. Dynamics of mitochondrial DNA evolution in animals:amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86 (16):6196-6200.
Lagos L, Bárcena F. 2018. Spatial variability in wolf diet and prey selection in Galicia (NW Spain). Mammal Research, 63 (2):125-139.
Li T Y, Chen X, Zhen R, Qiu J M, Qiu D C, Xiao N, Ito A, Wang H, Giraudoux P, Sako Y, Nakao M, Craig P S. 2010. Widespread coendemicity of human cystic and alveolar echinococcosis on the eastern Tibetan Plateau, northwest Sichuan/southeast Qinghai, China. Acta Tropica:Journal of Biomedical Sciences, 113 (3):248-256.
Liu Q X. 2009. Activity rhythm, home range and habitat selection of the Tibetan fox. Ph. D thesis. Shanghai:East China Normal University. (in Chinese)
Liu Q X, Harris R B, Wang X M. 2010. Food habits of the Tibetan fox (Vulpes ferrilata) in the Kunlun Mountains, Qinghai Province, China. Mammalian Biology, 75 (3):283-286.
Macarthur R, Pianka E. 1966. On optimal use of a patchy environment. The American Naturalist, 100 (916):603-609.
Mallon D, Harris R B, Wegge P. 2016. Snow leopard prey and diet.In:Mccarthy T, Mallon D eds. Snow Leopards. Academic Press, 43-55.
Meng F. 2022. A study on the cold tolerance in Rana kukunoris. Master thesis. Lanzhou:Lanzhou University. (in Chinese)
Monterroso P, Godinho R, Oliveira T, Ferreras P, Kelly M J, Morin D J, Waits L P, Alves P C, Mills L S. 2019. Feeding ecological knowledge:the underutilised power of faecal DNA approaches for carnivore diet analysis. Mammal Review, 49 (2):97-112.
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. Molecular Ecology, 21 (8):1931-1950.
R Core Team. 2022. R:A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Schaller G B. 1998. Wildlife of the Tibetan Steppe. Chicago:University of Chicago Press, 186-189.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W S, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology, 12 (6):R60.
Shao X N, Song D Z, Huang Q W, Li S, Yao M. 2019. Fast surveys and molecular diet analysis of carnivores based on fecal DNA and metabarcoding. Biodiversity Science, 27 (5):543-556. (in Chinese)
Shao X N, Lu Q, Xiong M Y, Bu H L, Shi X Y, Wang D J, Zhao J D, Li S, Yao M. 2021. Prey partitioning and livestock consumption in the world's richest large carnivore assemblage. Current Biology, 31 (22):4887-4897.
Shehzad W, Riaz T, Nawaz M A, Miquel C, Poillot C, Shah S A, Pompanon F, Coissac E, Taberlet P. 2012. Carnivore diet analysis based on next-generation sequencing:application to the leopard cat (Prionailurus bengalensis) in Pakistan. Molecular Ecology, 21 (8):1951-1965.
Smith A T, Xie Y. 2009. A Guide to the Mammals of China. Changsha:Hunan Education Publishing House, 385-418. (in Chinese)
Śmietana W, Klimek A. 1993. Diet of wolves in the Bieszczady Mountains, Poland. Acta Theriologica, 38 (3):245-251.
Sun R Y, Wang D H, Niu C J. 2019. Principles of Animal Ecology.Beijing:Beijing Normal University Publishing Group, 150-160.(in Chinese)
Thompson I D, Wiebe P A, Mallon E, Rodgers A R, Fryxell J M, Baker J A, Reid D. 2014. Factors influencing the seasonal diet selection by woodland caribou (Rangifer tarandus tarandus) in boreal forests in Ontario. Canadian Journal of Zoology, 93 (2):87-98.
Tsukada H, Li W, Duo H, Guo Z H, Fu Y, Peng M, Shen X Y, Jing J W, Yuan A S, Ni M, He S D, Huang F Q, Feng K, Ishikawa K, Kobayashi I, Shinohara A, Nonaka N. 2014. A comparison of the diet and fine-scale distribution of sympatric Tibetan and red foxes in Qinghai, PR China. Wildlife Biology, 20 (6):356-361.
Wang G L, Yin H B. 2008. Advances on foraging behavioral ecology in nonhuman primates. Journal of Biology, 25 (5):10-12. (in Chinese)
Wang X, Liu J Y, Zuo Q Q, Mu Z Q, Weng X D, Sun X H, Wang J Y, Boufana B, Craig P S, Giraudoux P, Raoul F, Wang Z H. 2018.
Echinococcus multilocularis and Echinococcus shiquicus in a small mammal community on the eastern Tibetan Plateau:host species composition, molecular prevalence, and epidemiological implications. Parasites & Vectors, 11 (1):302.
Wu Y G, Ye Z L, Wu Y S, Xu D M, Zou R F. 2017. Activity patterns of Lophura nycthemera based on camera trap data. Sichuan Journal of Zoology, 36 (1):25-29. (in Chinese)
Xiong M Y, Wang D J, Bu H L, Shao X N, Zhang D, Li S, Wang R J, Yao M. 2017. Molecular dietary analysis of two sympatric felids in the Mountains of Southwest China biodiversity hotspot and conservation implications. Scientific Reports, 7 (1):41909.
Zheng S W. 1985. Data on the foods of Tibetan sand fox. Acta Theriologica Sinica, 5 (3):222-240. (in Chinese)
Zhou Y Y. 2021. The relationship between habitat selection and snowfall for plateau pika. Master thesis. Lanzhou:Lanzhou University. (in Chinese)
Zou R J, Ji W Z, Yang S C, Tian B P, Bao H X, Tu J P, Zhou H W. 1994. A preliminary study on breeding Yunnan snub-nosed monkeys (Rhinopithecus bieti). Zoological Research, 15 (2):87-92.(in Chinese)
Zuo Q Q. 2022. The role of Tibetan fox-glires food chain in the transmission of echinococcosis in the eastern Tibetan Plateau. Ph. D thesis. Shanghai:East China Normal University. (in Chinese)
Smith A T, 谢焱. 2009. 中国兽类野外手册. 长沙:湖南教育出版社, 385-418.
王贵林, 尹华宝. 2008. 非人灵长类觅食行为生态学研究进展. 生物学杂志, 25 (5):10-12.
中华人民共和国国家卫生健康委员会. 2010. 防治包虫病行动计划 (2010-2015 年).[12. 04]. http://www.gov.cn/gzdt/2010-12/14/content_1765483.htm
左清秋. 2022. 青藏高原东部牧区藏狐-啮齿类动物食物链在棘球蚴病传播中的作用. 上海:华东师范大学博士学位论文.
石渠县志编纂委员会. 2000. 石渠县志. 成都:四川人民出版社,65-72.
冯祚建, 蔡桂全, 郑昌琳. 1986. 西藏哺乳类. 北京:科学出版社, 132-134.
刘群秀. 2009. 藏狐的活动规律、家域特征及生境选择的研究. 上海:华东师范大学博士学位论文.
孙儒泳, 王德华, 牛翠娟. 2019. 动物生态学原理 (第 4 版). 北京:北京师范大学出版社, 150-160.
吴友贵, 叶珍林, 吴义松, 许大明, 周荣飞. 2017. 基于红外相机技术的野生白鹇活动规律. 四川动物, 36 (1):25-29.
邹如金, 季维智, 杨上川, 田保平, 保海仙, 屠建平, 周红武. 1994. 滇金丝猴驯养的初步研究. 动物学研究, 15 (2):87-92.
邵昕宁, 宋大昭, 黄巧雯, 李晟, 姚蒙. 2019. 基于粪便 DNA 及宏条形码技术的食肉动物快速调查及食性分析. 生物多样性, 27(5):543-556.
国家林业和草原局. 2021. 国家重点保护野生动物名录.[12. 04]. http://www.gov.cn/xinwen/2021-02/09/content_5586227.htm
周雨阳. 2021. 高原鼠兔的栖息地选择与降雪的关系. 兰州:兰州大学硕士学位论文.
郑生武. 1985. 藏狐的食性资料. 兽类学报, 5 (3):222-240.
孟菲. 2022. 高原林蛙低温耐受能力的研究. 兰州:兰州大学硕士学位论文.

[1]	BAI Xiaojie, XIAO Wenhong, ZHANG Tingyue, LIU Bangyou, XIAO Zhishu, LIU Wei. Seasonal variation patterns of daily activity rhythm of small Indian civets (Viverricula indica) and their potential rodent prey in Guizhou Chishui Alsophila National Nature Reserve, China [J]. ACTA THERIOLOGICA SINICA, 2024, 44(3): 309-320.
[2]	Ziqian LI, Yongliang ZHU, Linguo LI, Wei LI, Jianguang YANG, Zhenhua GUAN, Xuelong JIANG. The activity budget and the influencing factor of a monogamous western black crested gibbon (Nomascus concolor) group [J]. ACTA THERIOLOGICA SINICA, 2023, 43(2): 141-148.
[3]	TENG Yang, GAI Lixin, LI Jian, FANG Xinmin, YANG Nan, BAO Weidong. A comparison of two methods of leopard cat food content analysis [J]. ACTA THERIOLOGICA SINICA, 2023, 43(1): 50-58.
[4]	LIU Zheng, LIU Shengyuan, LI Youbang, HUANG Zhonghao. Positional behavior of Assam macaque (Macaca assamensis) living in the limestone forest of southwest Guangxi, China [J]. ACTA THERIOLOGICA SINICA, 2022, 42(1): 12-23.
[5]	LI Xingkang, ZHONG Xukai, WEI Shaogan, CUI Liangwei, FAN Pengfei, GUAN Zhenhua, MA Changyong. The influence of group size and foraging environment on the daily path length of a critically endangered primate Nomascus nasutus [J]. ACTA THERIOLOGICA SINICA, 2021, 41(4): 388-397.
[6]	ZHANG Zhao, ZHANG Rui, LI Xiaoyu, Saihan, YANG Zhendong, HAN Zhiqing, BAO Weidong. Genetic diversity and sex structure of red deer population in Saihanwula Nature Reserve, Inner Mongolia [J]. ACTA Theriologica Sinica, 2021, 41(1): 42-50.
[7]	ZHU Bowei, WANG Bin, RAN Jianghong, LI Bo, HUANG Feng, LI Xiaoqing, GU Xiaodong. Seasonal variation of daily activity patterns and diet of yellow-throated marten (Martes flavigula) [J]. ACTA THERIOLOGICA SINICA, 2019, 39(1): 52-61.
[8]	CUI Zhenwei, WANG Zhenlong, ZHAO Guoliang, LU Jiqi. Seasonal variations in activity budget of adult female rhesus macaques (Macaca mulatta) at Mt. Taihangshan area, Jiyuan, China: effects of diet and temperature [J]. ACTA THERIOLOGICA SINICA, 2015, 35(2): 138-146.
[9]	YANG Yingyuan, LIU Nan, ZUO Qingqiu, RENQING Pengcuo, XIE Fei, YANG Gang, WANG Zhenghuan. The screening of microsatellite DNA loci for the identification of individual Tibetan foxes,using copro-DNA samples [J]. ACTA THERIOLOGICA SINICA, 2014, 34(4): 387-.
[10]	LI Dayong,REN Baoping,HU Jie,HE Xinming,LI Baoguo,LI Ming. Time budgets of Rhinopithecus bieti at Xiangguqing in the Baimaxueshan National Nature Reserve,Northwest Yunnan,China [J]. , 2013, 33(3): 223-231.
[11]	ZHANG Mingchun,LI Zhigang,HU Tianhua,WANG Jifei,WANG Xiaoming. Distribution and group size of red deer (Cervus elaphus)in Ningxia He- lan Mountain National Nature Reserve,China [J]. , 2012, 32(4): 318-324.
[12]	LI Dayong,REN Baoping,HE Xinming,HU Gang,LI Baoguo,LI Ming. Diet of Rhinopithecus bieti at Xiangguqing in Baimaxueshan National Nature Reserve [J]. , 2011, 31(4): 338-346.
[13]	HUANG Zhonghao,ZHOU Qihai,HUANG Chengming,MENG Yuanjun,WEI Hua. Home range and daily ranging distance of Francois’ langur (Trachypithecus francoisi ) in Nonggang NatureReserve, Guangxi, China [J]. , 2011, 31(1): 46-54.
[14]	LIU Xiaoqing,WANG Xiaoming,WANG Zhenghuan,LIU Qunxiu,MA Bo. Comparison of the Tibetan fox (Vulpes ferrilata) home range size using methods the fixed kernel estimation and the minimum convex polygon [J]. , 2010, 30(2): 163-170.
[15]	HUA Yan,ZHANG Wei,XU Yanchun. Seasonal variation of pelage characteristics in Siberian weasel (Mustela sibirica) of Xiaoxing’anling area,Heilongjiang,China [J]. , 2010, 30(1): 110-114.