Effects of dietary protein contents on the immune function of plateau pika (Ochotona curzoniae)

doi:10.16829/j.slxb.150743

ACTA THERIOLOGICA SINICA ›› 2023, Vol. 43 ›› Issue (3): 293-303.DOI: 10.16829/j.slxb.150743

• ORIGINAL PAPERS • Previous Articles Next Articles

Effects of dietary protein contents on the immune function of plateau pika (Ochotona curzoniae)

Lu ZHANG¹^,², Xueqin WU¹^,², Huiqing CHEN¹^,², Xin DONG¹^,², Guozhen SHANG¹^,³(), Yan WU⁴, Jianghui BIAN¹^,³

^1.Key Laboratory of Adaptation and Evolution of Plateau, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China
^2.University of Chinese Academy of Science, Beijing 100049, China
^3.Qinghai Key Laboratory of Animal Ecological Genomics, Xining 810001, China
^4.School of Life and Environment Sciences, Hangzhou Normal University, Hangzhou 310012, China

Received:2022-10-25 Accepted:2023-02-06 Online:2023-05-31 Published:2023-05-18
Contact: Guozhen SHANG

食物蛋白质含量对高原鼠兔免疫功能的影响

张璐¹^,², 吴学琴¹^,², 陈慧青¹^,², 董昕¹^,², 尚国珍¹^,³(), 吴雁⁴, 边疆晖¹^,³

^1.中国科学院西北高原生物研究所，高原适应与进化重点实验室，西宁 810001
^2.中国科学院大学，北京 100049
^3.青海省动物生态基因组学重点实验室，西宁 810001
^4.杭州师范大学生命与环境科学学院，杭州 310012

通讯作者: 尚国珍
作者简介:张璐 (1998- )，女，硕士研究生，主要从事动物生理生态学研究；
吴学琴 (1995- )，女，博士研究生，主要从事动物生理生态学研究；
吴学琴 (1995- )，女，博士研究生，主要从事动物生理生态学研究；第一联系人： 共同第一作者
陈慧青 (1996- )，女，博士研究生，主要从事动物生理生态学研究.
基金资助:
青海省自然科学基金青年项目(2021-ZJ-945Q);国家自然科学基金(31870397);中国科学院A类先导专项(XDA2005010406);青海省人民政府中国科学院三江源国家公园联合专项(LHZX-2020-01)

Abstract

Abstract:

The plateau pika (Ochotona curzoniae) is not only a small herbivorous mammal unique to the Qinghai-Tibet Plateau, but also a keystone species in the alpine grassland ecosystem. The population number of plateau pikas has increased dramatically with the degradation of grasslands caused by overgrazing. Our recent research has found that the immune system of plateau pikas was significantly enhanced as the alpine grassland degrades, and speculated it maybe related to the rich high-protein food resources in the degraded alpine grassland. To further validate this hypothesis, a field experiment was conducted in a highly degraded grassland of the Qinghai Haibei National Field Research Station of Alpine Grassland Ecosystem. The objective of this study is to verify the hypothesis that rich high-protein food resources could increase the immune system of plateau pikas. Six sample plots (70 m × 70 m) were randomized amongst three treatment groups: no supplementation (control); supplementation with rabbit chow with 5% protein; and supplementation with rabbit chow with 20% protein. We measured the fecal cortisol metabolite (FCM) levels, phytohemagglutinin (PHA) response, IgG levels of keyhole limpet hemocyanin (KLH) in serum, and intestinal parasitic infection status of plateau pikas. The results showed that supplementation with pelleted chow with 20% protein treatment significantly decreased the FCM levels of plateau pikas, significantly increased the PHA response and IgG levels against KLH, and significantly reduced the infection rate of coccidia and the infection intensity of cestodes. This result confirmed the above hypothesis and suggested that in degraded alpine grasslands, high-protein food can promote the growth of plateau pika populations by alleviating the vicious cycle between stress-immunity-parasitic infections.

Key words: Food protein, Ochotona curzoniae, Immunity, Stress, Parasitic infections

摘要：

高原鼠兔 (Ochotona curzoniae) 不仅是青藏高原特有的小型植食性哺乳动物，也是高寒草地生态系统的关键物种，其种群数量随着过度放牧引起的草地退化而急剧增加。我们近期的研究发现，随着高寒草地退化，高原鼠兔的免疫力明显增强，推测可能与退化的高寒草地中丰富的高蛋白质食物资源有关。为了进一步验证上述推测，本研究在青海海北高寒草地生态系统国家野外科学观测研究站地区的重度退化草地中，选取6块70 m × 70 m的实验样地，通过添加蛋白质含量为20%和5%的兔颗粒饲料及不添加饲料处理，测定了高原鼠兔的粪便皮质醇 (Fecal cortisol metabolite, FCM) 含量、植物血凝素反应 (Phytohemagglutinin, PHA)、血清抗匙孔血蓝蛋白 (Keyhole limpet haemoeyanin, KLH) 的 IgG 水平含量和肠道寄生物感染状况，以验证丰富的高蛋白质食物资源可增加高原鼠兔的免疫力的假设。结果表明，添加20%蛋白质含量的饲料显著降低了高原鼠兔的FCM含量，显著增加了PHA反应和抗KLH的IgG含量，显著降低了球虫的感染率和绦虫的感染强度。该结果验证了上述假设，并认为在退化的高寒草地中，高蛋白质食物通过缓解高原鼠兔的应激―免疫―寄生物感染状况之间的恶性循环，从而促进高原鼠兔种群增长。

关键词: 食物粗蛋白质, 高原鼠兔 (Ochotona curzoniae), 免疫能力, 应激, 寄生物感染

CLC Number:

Q494

Lu ZHANG, Xueqin WU, Huiqing CHEN, Xin DONG, Guozhen SHANG, Yan WU, Jianghui BIAN. Effects of dietary protein contents on the immune function of plateau pika (Ochotona curzoniae)[J]. ACTA THERIOLOGICA SINICA, 2023, 43(3): 293-303.

张璐, 吴学琴, 陈慧青, 董昕, 尚国珍, 吴雁, 边疆晖. 食物蛋白质含量对高原鼠兔免疫功能的影响[J]. 兽类学报, 2023, 43(3): 293-303.

Figures/Tables 4

Fig. 1 Cortisol content of plateau pika under the treatment of adding feeds with different protein content. Different lowercase letters indicate significant differences (P < 0.05) between treatments in the consent trapping period, “*” indicates significant differences between trapping periods (P < 0.05), and in March, the sample sizes n = 11, 36, 48 for the control, 5% low protein groups, and 20% high protein groups, respectively; Correspondingly, n = 23, 84, 110 in July. Data were expressed as the mean ± SE

Fig. 2 PHA responses of plateau pikas under the treatment with different protein content feeds. Different lowercase letters indicate significant differences between treatments in the same trapping period (P < 0.05), and “ns”indicates non-significant differences between trapping periods (P > 0.05). In March, the sample sizes n = 14, 38, 56 for the control, 5% low protein groups, and 20% high protein groups, respectively; Correspondingly, n = 31, 80, 78 in July. Data were expressed as the mean ± SE

Fig. 3 Anti-KLH IgG level of plateau pika under supplement different diets of protein content treatments. Different capital letters indicate significant differences between treatments (P < 0.05).In March, the sample sizes n = 10, 23, 39 for the control, 5% low protein groups, and 20% high protein groups, respectively; Correspondingly, n = 13, 52, 59 in July. Data were expressed as the mean ± SE

Fig. 4 Prevalence (A) and intensity (D) of intestinal coccidia infection, prevalence (B) and intensity (E) of cestode infection, and prevalence (C) and intensity (F) of nematode infection in plateau pika. Different capital letters indicate significant differences between treatments (P < 0.05), and different lowercase letters indicate significant differences in the interaction of treatment and time (P < 0.05). In March, the sample sizes n = 8, 36, 63 for the control group, 5% low protein group, and 20% high protein group, respectively; Correspondingly, n = 13, 59, 78 in May, n = 26, 98, 124 in July, and n = 25, 83, 102 in September. Data were expressed as the mean ± SE

References 0

	Boonstra R, Krebs C J, Stenseth N C. 1998. Population cycles in small mammals: the problem of explaining the low phase. Ecology, 79 (5): 1479-1488.
	Bush A O, Lafferty K D, Lotz J M, Shostak A W. 1997. Parasitology meets ecology on its own terms: Margoliset al. revisited. The Journal of Parasitology, 575-583.
	Bises G, Mengheri E, Gaetani S. 1987. T-lymphocyte subsets in zinc deficient and in protein malnourished rats. Nutrition Reports International, 36 (6): 1371-1378.
	Bakker E, Olff H, Gleichman J. 2009. Contrasting effects of large herbivore grazing on smaller herbivores. Basic and Applied Ecology, 10 (2): 141-150.
	Bian J H, Wu Y, Zhou K K. 2008. Effects of population density on demography and individual corticosterone level during breeding period in root voles (Microtus oeconomus). Acta Theriologica Sinica, 28 (2): 135-143. (in Chinese)
	Bian J H, Fan N C, Jing Z C, Shi Y Z. 1994. Studies on the successive relation between small mammal community and plant community in alpine meadow. Acta Theriologica Sinica, 14 (3): 209-216. (in Chinese)
	Bian J H, Zeng J H, Liu J K. 2001. Infuence of group size and distance to refuge on foraging of plateau pikas under predation risk. Acta Theriologica Sinica, 21 (3): 187-194. (in Chinese)
	Cao Y, Tveten A K, Stene A. 2017. Establishment of a non‑invasive method for stress evaluation in farmed salmon based on direct fecal corticoid metabolites measurement. Fish & Shellfish Immunology, 66: 317-324.
	Cooper T, Trunkfield H, Zanella A, Booth W. 1989. An enzyme‑linked immunosorbent assay for cortisol in the saliva of man and domestic farm animals. Journal of Endocrinology, 123 (2): R13-R16.
	Corripio‑Miyar Y, Hayward A, Lemon H, Sweeny A R, Bal X, Kenyon F, Pilkington J G, Pemberton J M, Nussey D H, McNeilly T N. 2022. Functionally distinct T-helper cell phenotypes predict resistance to different types of parasites in a wild mammal. Scientific Reports, 12 (1): 1-12.
	Dai J X. 1990. Climate of Qinghai-Tibet Plateau. Beijing: China Meteorological Press, 125-188. (in Chinese)
	Davis R, Lochmiller R, Warde W. 1995. Splenocyte subpopulations of weanling cotton rats (Sigmodon hispidus) are influenced by moderate protein intake. Journal of Mammalogy, 76 (3): 912-924.
	Davidson A D, Ponce E, Lightfoot D C, Fredrickson E L, Brown J H, Cruzado J, Brown J C, Sandra L, Brantley, Rodrigo S C, Rurik L, David T, Gerardo C. 2010. Rapid response of a grassland ecosystem to an experimental manipulation of a keystone rodent and domestic livestock. Ecology, 91 (11): 3189-3200.
	De Bellocq J G, Krasnov B R, Khokhlova I S, Pinshow B. 2006. Temporal dynamics of a T-cell mediated immune response in desert rodents. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145 (4): 554-559.
	Demas G E, Nelson R J. 1996. Photoperiod and temperature interact to affect immune parameters in adult male deer mice: (Peromyscus manicuiatus). Journal of Biological Rhythms, 11 (2): 94-102.
	Dhabhar F S. 1998. Stress‑induced enhancement of cell‑mediated immunity. Annals of the New York Academy of Sciences, 840 (1): 359-372.
	Dixon F J, Jacot‑Guillarmod H, McConahey P J. 1966. The antibody responses of rabbits and rats to hemocyanin. The Journal of Immunology, 97 (3): 350-355.
	Du S Y, Cao Y F, Nie X H, Wu Y, Bian J H. 2016. The synergistic effect of density stress during the maternal period and adulthood on immune traits of root vole (Microtus oeconomus) individuals-a field experiment. Oecologia, 181 (2): 335-346.
	Dong Q M, Ma Y S, Li Q Y, Shi J J, Wang Q J. 2004. Effects of yaks stocking pates on aboveground and belowground blomass in kobrecia parva alpine meadow. Pratacultural Science, 21 (2): 48-53. (in Chinese)
	Frick L, Barreiro Arcos M, Rapanelli M, Zappia M, Brocco M, Mongini C, Genaro A, Cremaschi G. 2009. Chronic restraint stress impairs T-cell immunity and promotes tumor progression in mice. Stress, 12 (2): 134-143.
	Fan N C, Zhang D C. 1996. Foraging behavior of Ochotona curzoniae and Ochotona dauurica and their adaptation to habitat. Acta Theriologica Sinica, 16 (1): 48-53. (in Chinese)
	Feng F, Gong B C, Niu K C. 2015. Linking density of plateau pika to vegetation characteristics and soil attributes in response to different grazing regimes. Pratacultural Science, 36 (11): 2915-2925. (in Chinese)
	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.
	Hagenah N, Prins H H T, Olff H. 2009. Effects of large herbivores on murid rodents in a South African savanna. Journal of Tropical Ecology, 25: 483-492.
	Houdijk J G M, Jessop N S, Kyriazakis I. 2001. Nutrient partitioning between reproductive and immune functions in animals. Proceedings of the Nutrition Society, 60 (4): 515-525.
	Houdijk J G, Jessop N S, Knox D P, Kyriazakis I. 2005. Secondary infection of Nippostrongylus brasiliensis in lactating rats is sensitive to dietary protein content. British Journal of Nutrition, 93 (4): 493-499.
	Jones L, Houdijk J, Sakkas P, Bruce A, Mitchell M, Knox D, Kyriazakis I. 2011. Dissecting the impact of protein versus energy host nutrition on the expression of immunity to gastrointestinal parasites during lactation. International Journal for Parasitology, 41 (7): 711-719.
	Jiang Z G, Xia W P. 1985. Utilization of the food resources by plateau pika. Acta Theriologica Sinica, 5 (4): 13-24. (in Chinese)
	Kang L, Han X, Zhang Z, Sun O J. 2007. Grassland ecosystems in China: review of current knowledge and research advancement. Philosophical Transactions of the Royal Society B: Biological Sciences, 362 (1482): 997-1008.
	Książek A, Zub K, Szafrańska P A, Wieczorek M, Konarzewski M. 2014. Immunocompetence and high metabolic rates enhance overwinter survival in the root vole, Microtus oeconomus . Biology Letters, 10 (12): 20140684.
	Kim W H, Chaudhari A A, Lillehoj H S. 2019. Involvement of T cell immunity in avian coccidiosis. Frontiers in Immunology, 10: 2732.
	Krebs C J, Gilbert B S, Boutin S, Sinclair A R, Smith J N. 1986. Population biology of snowshoe hares. I. Demography of food-supplemented populations in the southern Yukon, 1976—1984. The Journal of Animal Ecology, 55: 963-982.
	Krebs C J. 2009. The lemming cycle at Baker Lake, N.W.T., during 1959-1961. Ecology, 14 (2): 91-100.
	Krebs C J, Boonstra R, Boutin S, Sinclair A R. 2001. What drives the 10‑year cycle of snowshoe hares? The ten‑year cycle of snowshoe hares-one of the most striking features of the boreal forest-is a product of the interaction between predation and food supplies, as large‑scale experiments in the Yukon have demonstrated. BioScience, 51 (1): 25-35.
	Kenney M A, Roderuck C E, Arnrich L, Piedad F. 1968. Effect of protein deficiency on the spleen and antibody formation in rats. The Journal of Nutrition, 95 (2): 173-178.
	Lewis J G, Manley L, Townsend J C, Elder P A. 1986. An enzyme‑linked immunosorbent assay (ELISA) for urinary free cortisol. Clinica Chimica Acta, 159 (2): 205-209.
	Li X C, Wang Z N, Wang D L, Wang L, Pan D F, Li J, De K J, Seastedt T R. 2019. Livestock grazing impacts on plateau pika (Ochotona curzoniae) vary by species identity. Agriculture, Ecosystems and Environment, 275: 23-31.
	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.
	Lochmiller R L, Vestey M R, Nash D. 1992. Gut associated lymphoid tissue in the cotton rat (Sigmodon hispidus) and its response to protein restriction. Journal of Wildlife Diseases, 28 (1): 1-9.
	Liu J K, Su J P, Liu W, Wang X, Nie H Y, Liu Y M. 1994. Field experimental studies on the multifactorial hypothesis of population system regulation for small rodents: an analysis of effects of food availability and predation on population dynamics of root vole. Acta Theriologica Sinica, 14 (2): 117-129. (in Chinese)
	Liu W, Zhang Y, Wang X, Zhao J Z, Xu Q M, Zhou L. 2008. Food selection by plateau pikas in different habitats during plant growing season. Acta Theriologica Sinica, 28 (4): 358-366. (in Chinese)
	Merlo J L, Cutrera A P, Zenuto R R. 2016. Parasite infection negatively affects PHA‐triggered inflammation in the subterranean rodent Ctenomys talarum . Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 325 (2): 132-141.
	Mihok S, Turner B N, Iverson S L. 1985. The characterization of vole population dynamics. Ecological Monographs, 55 (4): 399-420.
	Nelson R J, Demas G E. 1996. Seasonal changes in immune function. The Quarterly Review of Biology, 71 (4): 511-548.
	Nie X H, Cao Y F, Du S Y, He H, Bian J H. 2014. Intestinal parasites prevalence in root voles (Microtus oeconomus) from field enclosures. Acta Theriologica Sinica, 34 (2): 172-180. (in Chinese)
	Rose M E, Hesketh P. 1979. Immunity to coccidiosis: T-lymphocyte-or B-lymphocyte-deficient animals. Infection and Immunity, 26 (2): 630-637.
	Rose M E, Ogilvie B M, Hesketh P, Festing M. 1979. Failure of nude (athymic) rats to become resistant to reinfection with the intestinal coccidian parasite Eimeria nieschulzi or the nematode Nippostrongylus brasiliensis . Parasite Immunology, 1 (2): 125-132.
	Ren Q J, Wu G L, Ren G H. 2009. Effect of grazing intensity on characteristics of alpine meadow communities in the eastern Qinghai-Tibetan Plateau. Pratacultural Science, 18 (5): 256-261. (in Chinese)
	Schaller G B. 2000. Wildlife of the Tibetan Steppe. University of Chicago Press.
	Shang G Z, Zhu Y H, Wu Y, Cao Y F, Bian J H. 2019. Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia, 191 (1): 83-96.
	Sheriff M J, Bosson C O, Krebs C J, Boonstra R. 2009. A non‑invasive technique for analyzing fecal cortisol metabolites in snowshoe hares (Lepus americanus). Journal of Comparative Physiology B, 179 (3): 305-313.
	Shimada M, Takahashi K, Ohkawa T, Segawa M, Higurashi M. 1995. Determination of salivary cortisol by ELISA and its application to the assessment of the circadian rhythm in children. Hormone Research in Paediatrics, 44 (5): 213-217.
	Sinclair J, Lochmiller R. 2000. The winter immunoenhancement hypothesis: associations among immunity, density, and survival in prairie vole (Microtus ochrogaster) populations. Canadian Journal of Zoology, 78 (2): 254-264.
	Smith A T, Foggin J M. 1999. The Plateau Pika (Ochotona curzoniae) is a Keystone Species for Biodiversity on the Tibetan Plateau. Animal Conservation Forum.Cambridge University Press, 2 (4): 235-240.
	Smith A T, Wilson M C, Hogan B W. 2019. Functional‐trait ecology of the plateau pika (Ochotona curzoniae) in the Qinghai-Tibetan Plateau ecosystem. Integrative Zoology, 14 (1): 87-103.
	Speakman J R, Chi Q, Ołdakowski Ł, Fu H, Fletcher Q E, Hambly C, Togo J, Liu X, Piertney S B, Wang X. 2021. Surviving winter on the Qinghai-Tibetan Plateau: pikas suppress energy demands and exploit yak feces to survive winter. Proceedings of the National Academy of Sciences, 118 (30): e2100707118.
	Stear M, Bishop S, Doligalska M, Duncan J, Holmes P, Irvine J, McCririe L, McKellar Q, Sinski E, Murray M. 1995. Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta . Parasite Immunology, 17 (12): 643-652.
	Shi Y Z. 1983. On the influences of range land vegetation to the density of plateau pika (Ochotona curzoniae). Acta Theriologica Sinica, 3 (2): 181-187. (in Chinese)
	Vestey M, McMurry S, Lochmiller R. 1993. Influence of dietary protein on selected measures of humoral and cellular immunity in the cotton rat Sigmodon hispidus . Canadian Journal of Zoology, 71 (3): 579-586.
	Wakelin D, Rose M, Hesketh P, Else K, Grencis R. 1993. Immunity to coccidiosis: genetic influences on lymphocyte and cytokine responses to infection with Eimeria vermiformis in inbred mice. Parasite Immunology, 15 (1): 11-19.
	Wasser S, Thomas R, Nair P, Guidry C, Southers J, Lucas J, Wildt D, Monfort S. 1993. Effects of dietary fibre on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). Reproduction, 97 (2): 569-574.
	Watson R R, Haffer K. 1980. Modifications of cell-mediated immune responses by moderate dietary protein stress in immunologically immature and mature BALB/c mice. Mechanisms of Ageing and Development, 12 (3): 269-278.
	Wetzel R. 1951. Verbesserte McMaster-Kammer zum Auszhlen von Wurmeiern. Tierärztl Umsch, 6: 209-210.
	Wilson M C. 2015. The pika and the watershed: the impact of small mammal poisoning on the ecohydrology of the Qinghai-Tibetan Plateau. AMBIO, 44 (1): 16-22.
	Woodward B D, Miller R G. 1991. Depression of thymus-dependent immunity in wasting protein-energy malnutrition does not depend on an altered ratio of helper (CD4+) to suppressor (CD8+) T cells or on a disproportionately large atrophy of the T‑cell relative to the B‑cell pool. The American Journal of Clinical Nutrition, 53 (5): 1329-1335.
	Wang X, Liu J K, Liu W, Ji L J. 1992. Studies on the nutrition alecology of herbivorous small mammals: patterns of food selection and food quality for plateau pikas, Ochotona curzoniae . Acta Theriologica Sinica, 12 (3): 183-192. (in Chinese)
	Wang X T, Zhang S H, Chen D D, Tan Y R, Sun D S, Du G Z. 2010. The effects of natural grazing intensity on plant community and soil nutrients in alpine meadow. Acta Agrestia Sinica, 18 (4): 510-516. (in Chinese)
	Wu X Q, Chen H Q, Zhang L, Shang G Z, Wu Y, Bian J H. 2022. Grassland degradation affects serum total IgG level, intestinal parasitic infection and liver and kidney indices of plateau pika. Acta Theriologica Sinica, 42 (5): 531-539.(in Chinese)
	Xu D L, Wang D H. 2010. Fasting suppresses T cell‑mediated immunity in female Mongolian gerbils (Meriones unguiculatus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 155 (1): 25-33.
	Xu D, Liu X, Wang D. 2011. Impairment of cellular and humoral immunity in overweight Mongolian gerbils (Meriones unguiculatus). Integrative Zoology, 6 (4): 352-365.
	Yang Y B, Shang G Z, Du S Y, Zhang X, Bian J H. 2018. Maternal density stress and coccidian parasitism: synergistic effects on overwinter survival in root voles. Functional Ecology, 32 (9): 2181-2193.
	Zhou H K, Zhou L, Zhao X Q, Yan Z L, Liu W, Shi Y. 2002. Influence of grazing disturbance on alpine grassland. Grassland of China, 24 (5): 54-62. (in Chinese)
	Zhang Z Q, Wang D H. 2005. Animal immunocompetence and its effect on population regulation an d life history trade‑off. Chinese Journal of Applied Ecology, 16 (7): 1375-1379. (in Chinese)
	Zhang F L, Wei W R, Gao S Y, Zhang W G. 2005. The effects of plant community structure on population density of plateau pikas (Ochotona curzoniae) in alpine meadow grassland. Acta Prataculturae Sinica, 28 (3): 93-100. (in Chinese)
	仁青吉, 武高林, 任国华. 2009. 放牧强度对青藏高原东部高寒草甸植物群落特征的影响. 草业学报, 18 (5): 256-261.
	王溪, 刘季科, 刘伟, 纪兰菊. 1992. 植食性小哺乳类营养生态学的研究: 高原鼠兔的食物选择模式与食物质量. 兽类学报, 12 (3): 183-192.
	王向涛, 张世虎, 陈懂懂, 谈嫣蓉, 孙大帅, 杜国祯. 2010. 不同放牧强度下高寒草甸植被特征和土壤养分变化研究. 草地学报, 18 (4): 510-516.
	边疆晖, 樊乃昌, 景增春, 施银柱. 1994. 高寒草甸地区小哺乳动物群落与植物群落演替关系的研究. 兽类学报, 14 (3): 209-216.
	边疆晖, 景增春, 刘季科. 2001. 相关风险因子对高原鼠兔摄食行为的影响. 兽类学报, 21 (3): 187-194.
	边疆晖, 吴雁, 周抗抗. 2008. 繁殖期根田鼠种群密度对其种群统计参数及个体皮质酮水平的作用. 兽类学报, 28 (2): 135-143.
	冯峰, 贡保草, 牛克昌. 2019. 不同放牧模式下高原鼠兔密度与高寒植被和土壤的关系.草业科学, 36 (11): 2915-2925.
	刘季科, 苏建平, 刘伟, 王溪, 聂海燕, 李玉敏. 1994. 小型啮齿动物种群系统调节复合因子理论的野外实验研究: 食物可利用性和捕食对根田鼠种群动态作用的分析. 兽类学报, 14 (2): 117-129.
	刘伟, 张毓, 王溪, 赵建中, 许庆民, 周立. 2008. 植物生长季节不同栖息地高原鼠兔的食物选择. 兽类学报, 28 (4): 358-366.
	张志强, 王德华. 2005. 免疫能力与动物种群调节和生活史权衡的关系. 应用生态学报, 16 (7): 1375-1379.
	张灵菲, 卫万荣, 石高宇, 张卫国. 2019. 高寒草甸植物群落结构对高原鼠兔种群密度的影响.草业学报, 28 (3): 93-100.
	吴学琴, 陈慧青, 张璐, 尚国珍, 吴雁, 边疆晖. 2022. 草地退化影响高原鼠兔血清总IgG水平、肠道寄生物感染及肝脏和肾脏指数. 兽类学报, 42 (5): 531-539.
	周华坤, 周立, 赵新全, 严作良, 刘伟, 师燕. 2002. 放牧干扰对高寒草场的影响. 中国草地, 24 (5): 54-62.
	施银柱. 1983. 草场植被影响高原鼠兔密度的探讨. 兽类学报, 3 (2): 181-187.
	聂绪恒, 曹伊凡, 堵守杨, 何慧, 边疆晖. 2014. 野外围栏条件下根田鼠肠道寄生物的感染率. 兽类学报, 34 (2): 172-180.
	董全民, 马玉寿, 李青云, 施建军, 王启基. 2004. 牦牛放牧强度对高寒草甸暖季草场植被的影响. 草业科学, 21 (2): 48-53.
	蒋志刚, 夏武平. 1985. 高原鼠兔食物资源利用的研究. 兽类学报, 5 (4): 13-24.
	樊乃昌, 张道川. 1996. 高原鼠兔与达乌尔鼠兔的摄食行为及对栖息地适应性的研究. 兽类学报, 16 (1): 48-53.
	戴加洗. 1990. 青藏高原气候. 北京: 气象出版社, 125-188.

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Effects of dietary protein contents on the immune function of plateau pika (Ochotona curzoniae)

食物蛋白质含量对高原鼠兔免疫功能的影响

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