Grassland degradation affects serum total IgG level, intestinal parasitic infection and liver and kidney indices of plateau pika

doi:10.16829/j.slxb.150715

Abstract

Abstract:

As a key species in the alpine grassland ecosystem of the Qinghai?Tibet Plateau, the plateau pika (Ochotona curzoniae) population increased rapidly with grassland degradation. Understanding the changes in innate immune function and organ index of liver and kidney indices of plateau pika is of great significance for further revealing the physiological mechanism of plateau pika population outbreak caused by grassland degradation on the Qinghai?Tibet Plateau. In this study, we investigated the number of burrow entrances, measured serum total IgG levels, intestinal parasitic infection, and liver and kidney indices of adult plateau pikas inhabiting lightly, moderately, and heavily degraded grassland (LD, MD and HD) at Qinghai Haibei National Field Research Station of Alpine Grassland Ecosystem. Our results showed that with grassland degradation, the number of burrow entrances and serum total IgG levels increased significantly, while the prevalence and intensity of infection of cestodes and nematodes as well as liver and kidney indices decreased markedly. The prevalence of infection of cestodes and liver index in males were significantly lower than those in females, and the prevalence and intensity of infection of cestodes and nematodes in females in HD were significantly lower than those in LD. These results indicate that grassland degradation induced by overgrazing enhances the innate immune of plateau pika and alleviate the damage of toxins to liver and kidney, which may promote population outbreaks.

Key words: Plateau pika (Ochotona curzoniae), Grassland degradation, Food protein, Innate immune, Intestinal parasites, Population outbreaks

摘要：

高原鼠兔 (Ochotona curzoniae) 作为青藏高原高寒草地生态系统中的关键物种，其种群数量随着过度放牧导致的草地退化而暴发式增长。阐明此过程中高原鼠兔天然免疫能力及肝脏和肾脏器官指数的变化，对深入揭示青藏高原草地退化引起的高原鼠兔种群暴发机理具有重要意义。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，调查了轻度、中度、重度退化草地中高原鼠兔洞口数量，并测定了成体高原鼠兔血清总IgG含量、肠道寄生物感染状况及肝脏和肾脏指数。结果发现：随着草地退化，高原鼠兔洞口数量和血清总IgG水平显著增加；绦虫和线虫的感染率和感染强度以及肝脏和肾脏指数均显著降低。雄性对绦虫的感染率和肝脏指数显著低于雌性；雌性在重度退化草地中对绦虫和线虫的感染率及感染强度显著低于轻度退化草地。以上结果表明，过度放牧介导的草地退化增强了高原鼠兔的天然免疫功能，缓解了毒素对肝脏和肾脏的损伤，进而可能促进其种群暴发式增长。

关键词: 高原鼠兔, 草地退化, 食物蛋白, 天然免疫, 肠道寄生物, 种群暴发

CLC Number:

Q143

Xueqin WU, Huiqing CHEN, Lu ZHANG, Guozhen SHANG, Yan WU, Jianghui BIAN. Grassland degradation affects serum total IgG level, intestinal parasitic infection and liver and kidney indices of plateau pika[J]. ACTA THERIOLOGICA SINICA, 2022, 42(5): 531-539.

吴学琴, 陈慧青, 张璐, 尚国珍, 吴雁, 边疆晖. 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[J]. 兽类学报, 2022, 42(5): 531-539.

Figures/Tables 4

Fig. 1 The number of burrow entrances of plateau pika in lightly (LD), moderaterly (MD) and heavily degraded grassland (HD) (mean ± SE). The lowercase indicates significant difference (P < 0.05)

Fig. 2 Serum total IgG levels of plateau pika in LD, MD and HD (mean ± SE). n = 17, 25 and 23 for males and n = 26, 33 and 20 for females in LD, MD and HD, respectively. The lowercase indicates significant difference (P < 0.05). For abbreviations, see Fig.1

Fig. 3 Prevalence and intensity of intestinal parasites infection of plateau pika in LD, MD and HD (mean ± SE). n = 12, 11 and 11 for males and n = 13, 19 and 10 for females in LD, MD and HD, respectively. The lowercase indicates significant difference (P < 0.05). Because all the plateau pikas were infected with coccidia, the coccidian prevalence was not analyzed. The plateau pikas in MD were not infected with cestode, so the group was excluded during the statistical analyses. For abbreviations, see Fig.1

Fig. 4 The liver and kidney indices of plateau pika in LD, MD and HD (mean ± SE). n = 22, 30 and 28 for males and n = 32, 41 and 29 for females in LD, MD and HD, respectively. The lowercase indicates significant difference (P < 0.05). For abbreviations, see Fig.1

References 0

	Arsenault R, Owen‑Smith N. 2002. Facilitation versus competition in grazing herbivore assemblages. Oikos, 97 (3): 313-318.
	Bai Y L, Wu Y H, Han X H. 1999. Study on the relationship between the plant age and the nutrient component of alfalfa. Pratacultural Science, 16 (1): 18-21. (in Chinese)
	Bertolino S, Wauters L A, De Bruyn L, Canestri‑Trotti G. 2003. Prevalence of coccidia parasites (Protozoa) in red squirrels (Sciurus vulgaris): effects of host phenotype and environmental factors. Oecologia, 137 (2): 286-295.
	Bian J H, Cao Y F, Du Y, Yang L, Jing Z C. 2011. Effects of Parasitic Eimerians (Eimeria cryptobarretti and E. klondikensis) on mortality of plateau pika (Ochotona curzoniae). Acta Theriologica Sinica, 31 (3): 299-305. (in Chinese)
	Bian J H, Fan N C. 1997. The effect of predation risk on animals’behavior and their decision. Chinese Journal of Ecology, 16 (1): 34-39. (in Chinese)
	Bian J H, Jing Z C, Fan N C, Zhou W Y. 1999. Influence of cover on habitatutilization of plateau pika (Ochotona curzoniae). Acta Theriologica Sinica, 19 (3): 212-220. (in Chinese)
	Bian J H, Wu Y, Liu J K. 2005. Effect of predator‑induced maternal stress during gestation on growth in root voles Microtus oeconomus . Acta Theriologica, 50 (4): 473-482.
	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. Journal of Parasitology, 83 (4): 575-583.
	Caldwell J. 1982. Conjugation reactions in foreign‑compound metabolism: definition, consequences, and species variations. Drug Metabolism Reviews, 13 (5): 745-777.
	Cao Y F, Du Y, Yang L, Bian J H. 2011. Two new record species of eimeria (Apoicomplexa, Eimeriidae) from plateau pika in China. Sichuan Journal of Zoology, 30 (3): 402-403. (in Chinese)
	Cheng E, Ritchie M E. 2006. Impacts of simulated livestock grazing on Utah prairie dogs (Cynomys parvidens) in a low productivity ecosystem. Oecologia, 147 (3): 546-555.
	Cornell S J, Bjornstad O N, Cattadori I M, Boag B, Hudson P J. 2008. Seasonality, cohort‑dependence and the development of immunity in a natural host‑nematode system. Proceedings of the Royal Society B: Biological Sciences, 275 (1634): 511-518.
	Dai X, Gu X Z, Shi J, Yuan F, Yin B F, Wang A Q, Wei W H, Yang S M. 2012. The seasonal changes of plant secondary metabolites and their influence on the food selection of plateau pika. Acta Theriologica Sinica, 32 (4): 306-317. (in Chinese)
	Davis R, Lochmiller R I. 1995. Splenocyte subpopulation of weanling cotton rats (Signodon hispidus) are influenced by moderate protein intakes. Journal of Mammalogy, 76: 912-924.
	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.
	Duan C R, Wang B C, Xu S R. 2003. The effects of the environment stress on the plant secondary metabolites. Journal of Chongqing University, 26 (10): 67-71. (in Chinese)
	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)
	Foley W J. 1992. Nitrogen and energy retention and acid-base status in the common ringtail possum (Pseudocheirus peregrinus): evidence of the effects of absorbed allelochemicals. Physiological Zoology, 65 (2): 403-421.
	Forbes K M, Mappes T, Sironen T, Strandin T, Stua P, Meri S, Vapalahti O, Henttonen H, Huitu O. 2016. Food limitation constrains host immune responses to nematode infections. Biology Letters, 12 (9): 20160471.
	Forbes K M, Stuart P, Mappes T, Hoset K S, Henttonen H, Huitu O. 2014. Diet quality limits summer growth of field vole populations. PLoS ONE, 9 (3): e91113.
	Frank M M, Miletic V D, Jiang H X. 2000. Immunoglobulin in the control of complement action. Immunologic Research, 22 (2): 137-146.
	Greives T J, McGlothlin J W, Jawor J M, Demas G E, Ketterson E D. 2006. Testosterone and innate immune function inversely covary in a wild population of breeding Dark‑Eyed Juncos (Junco hyemalis). Functional Ecology, 20 (5): 812-818.
	Guo Z H, Jiang Q Q, Wang B, Zhao N, He Z F, Li H J, Lü J Z. 2022. Effect of lighting rhythm on growth performance, serum biochemical indexes, meat quality and welfare of rabbits. Acta Veterinaria Et Zootechnica Sinica, 53 (5): 1500-1508. (in Chinese)
	Hawley D M, Altizer S M. 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology, 25 (1): 48-60.
	He L, Li J N, Yang D M, Tao S L. 2010. Effects of plant phenolic compound on the growth and organ development of reed voles (Microtus fortis). Acta Theriologica Sinica, 30 (3): 297-303. (in Chinese)
	Holt R D, Roy M. 2007. Predation can increase the prevalence of infectious disease. The American Naturalist, 169 (5): 690-699.
	Jiang Z G, Xia W P. 1985. Utilization of the food resources by plateau pika. Acta Theriologica Sinica, 5 (4): 251-262. (in Chinese)
	Krueger K. 1986. Feeding relationships among bison, pronghorn, and prairie dogs: an experimental analysis. Ecology, 67 (3): 760-770.
	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.
	Lai D Z, Sun B C, He Y L, Ma Y S, Dong Q M. 2006. Reproduction traits and population amount of plateau pika in Guoluo region. Chinese Qinghai Journal of Animal and Veterinary Sciences, 36 (2): 4-6. (in Chinese)
	Li J N, Liu J K, Tao S L. 2003a. Effects of tannic acid on the food intake and protein digestibility of root voles. Acta Theriologica Sinica, 23 (1): 52-57. (in Chinese)
	Li J N, Liu J K, Tao S L. 2003b. Metabolic costs (Microtus oeconomus) of tannic acid in root voles. Acta Ecologica Sinica, 23 (9): 1816-1822. (in Chinese)
	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 & Environment, 275: 23-31.
	Lindroth R L, Batzli G O.1983. Detoxication of some naturally occuring phenolics by prairie voles: a rapid assay of glucuronidation metabolism.Biochemical Systematics and Ecology, 11 (4): 405-409.
	Liu Q S, Wang D H. 2004. Coprophagy in herbivorous small mammals. Acta Theriologica Sinica, 24 (3): 333-338. (in Chinese)
	Liu Q S, Wang D H. 2007. Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus). Journal of Comparative Physiology B, 177 (5): 509-518.
	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)
	Lochmiller R L, Deerenberg C. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88 (1): 87-98.
	Lochmiller R L, Vestey M R, Boren J C. 1993. Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. The Auk, 110 (3): 503-510.
	Lochmiller R L. 1996. Immunocompetence and animal population regulation. Oikos, 76 (3): 594-602.
	Lord G M, Matarese G, Howard J K, Baker R J, Bloom S R, Lechler R I. 1998. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature, 394 (6696): 897-901.
	Mihok S, Turner B N, Iverson S L. 1985. The characterization of vole population dynamics. Ecological Monographs, 55 (4): 399-420.
	Nelson R J. 2004. Seasonal immune function and sickness responses. Trends in Immunology, 25 (4): 187-192.
	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)
	Nohr C W, Tchervenkov J I, Meakins J L, Christou N V. 1985. Malnutrition and humoral immunity: short‑term acute nutritional deprivation. Surgery, 98 (4): 769-776.
	Nordling D, Andersson M, Zohari S, Lars G. 1998. Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265 (1403): 1291-1298.
	Ochsenbein A F, Zinkernagel R M. 2000. Natural antibodies and complement link innate and acquired immunity. Immunology Today, 21 (12): 624-630.
	Rickert R C. 2005. Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Current Opinion in Immunology, 17 (3): 237-243.
	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, Krebs C J, Boonstra R. 2010. Assessing stress in animal populations: Do fecal and plasma glucocorticoids tell the same story?General and Comparative Endocrinology , 166 (3): 614-619.
	Sheriff M J, Krebs C J, Boonstra R. 2011. From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle. Oecologia, 166 (3): 593-605.
	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)
	Sinclair J A, Lochmiller R L. 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, Badingqiuying, 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.
	Smith A T, Foggin J M. 1999. The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan Plateau. Animal Conservation, 2 (4): 235-240.
	Wetzel R. 1951. Verbesserte mcmaster-kammer zum auszählen von wurmeiern. Tierärztl Umsch, 6: 209-210.
	Wilson M C, Smith A T. 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.
	Xu D L, Wang D H. 2015. Effect of fasting duration on immune function in female Mongolian gerbils (Meriones unguiculatus). Acta Theriologica Sinica, 35 (4): 369-378. (in Chinese)
	Xu Y C, Yang D B, Wang D H. 2012. No evidence for a trade-off between reproductive investment and immunity in a rodent. PLoS ONE, 7 (5): e37182.
	Yang Y B, Shang G Z, Du S Y, Zhang X, Wu Y, Bian J H. 2018. Maternal density stress and coccidian parasitism: Synergistic effects on overwinter survival in root voles. Functional Ecology, 32 (9): 2181-2193.
	Ye N N. 2015. Effects of plant secondary metabolites on the feeding behavior of plateau pika. Master thesis. Lanzhou: Lanzhou University. (in Chinese)
	Zhang M, Wu Y H, Zhou X Q, Zhou H N. 2012. The effects of endosulfan on the growth and erythrocyte immune function of Mongolian gerbils (Meriones unfuiculatus). Immunopharmacology and Immunotoxicology, 34 (5): 754-762.
	Zhang Z Q, Wang D H. 2005. Animal immunocompetence and its effect on population regulation and life history trade-off. Chinese Journal of Applied Ecology, 16 (7): 1375-1379. (in Chinese)
	Zhang Z Q, Zhang L N, Wang D H. 2007. Effect of reducing photo period and temperature on energy metabolism and body composition in Brandt’s voles (Lasiopodomys brandtii). Acta Theriologica Sinica, 27 (1): 18-25. (in Chinese)
	Zhou L, Liu J K, Liu Y. 1987. Study on population productivity ecology of the plateau pika Ⅰ.A dynamic model of growth of body weight in the plateau pika. Acta Theriologica Sinica, 7 (1): 67-78. (in Chinese)
	白玉龙, 乌艳虹, 韩晓华. 1999. 紫花苜蓿株龄与其营养成分关系的研究. 草业科学, 16 (1): 18-21.
	边疆晖, 曹伊凡, 杜寅, 杨乐, 景增春. 2011. 艾美尔混合球虫对高原鼠兔致死毒力的初步研究. 兽类学报, 31 (3): 299-305.
	边疆晖, 景增春, 樊乃昌, 周文扬. 1999. 地表覆盖物对高原鼠兔栖息地利用的影响. 兽类学报, 19 (3): 212-220.
	边疆晖, 樊乃昌, 景增春, 张道川. 1994. 高原鼠兔和甘肃鼠兔摄食行为及其对栖息地适应性的研究.中国动物学会成立60周年：纪念陈桢教授诞辰100周年论文集.北京: 中国科学技术出版社, 403-408.
	边疆晖, 樊乃昌. 1997. 捕食风险与动物行为及其决策的关系. 生态学杂志, 16 (1): 34-39.
	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.
	刘全生, 王德华. 2004. 草食性小型哺乳动物的食粪行为. 兽类学报, 24 (3): 333-338.
	李俊年, 刘季科, 陶双伦. 2003a. 单宁酸对根田鼠食物摄入量和蛋白质消化率的效应. 兽类学报, 23 (1): 52-57.
	李俊年, 刘季科, 陶双伦. 2003b. 根田鼠对食物单宁酸的解毒代价. 生态学报, 23 (9): 1816-1822.
	李富娟, 玉永雄. 2006. 苜蓿蛋白质及影响苜蓿粗蛋白含量的主要因素. 四川草原, (2): 6-9.
	来德珍, 孙宝琛, 贺有龙, 马玉寿, 董全民. 2006. 果洛地区高原鼠兔繁殖特性种群数量和对天然草地的危害. 青海畜牧兽医杂志, 36 (2): 4-6.
	何岚, 李俊年, 杨冬梅, 陶双伦. 2010. 植物酚类化合物对东方田鼠体重增长和内脏器官发育的作用. 兽类学报, 30 (3): 297-303.
	冶娜娜. 2015. 植物次生代谢物对高原鼠兔采食行为的影响. 兰州大学硕士学位论文.
	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.
	张志强, 张丽娜, 王德华. 2007. 渐变的光周期和温度对布氏田鼠能量代谢和身体成分的影响. 兽类学报, 27 (1): 18-25.
	周立, 刘季科, 刘阳. 1987.高原鼠兔种群生产量生态学的研究 Ⅰ.高原鼠兔体重生长动态数学模型的研究.兽类学报, 7 (1): 67-78.
	段传人, 王伯初, 徐世荣. 2003. 环境应力对植物次生代谢产物形成的作用. 重庆大学学报, 26 (10): 67-71.
	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.
	徐德立, 王德华. 2015. 禁食时间对雌性长爪沙鼠免疫功能的影响. 兽类学报, 35 (4): 369-378.
	郭子涵, 蒋琪琪, 王彬, 赵娜, 贺稚非, 李洪军, 吕景智. 2022. 光照节律对肉兔生长性能, 血清生化指标, 肉品质和动物福利的影响. 畜牧兽医学报, 53 (5): 1500-1508.
	曹伊凡, 杜寅, 杨乐, 边疆晖. 2011. 高原鼠兔寄生艾美耳球虫 (顶复器门, 艾美耳科) 二中国新纪录种. 四川动物, 30 (3): 402-403.
	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): 251-262.
	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.
	戴鑫, 顾新州, 石佳, 袁飞, 殷宝法, 王爱勤, 魏万红, 杨生妹. 2012. 植物次生代谢物含量的季节性变化及其对高原鼠兔食物选择的影响. 兽类学报, 32 (4): 306-317.

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