普氏原羚警戒行为和生理应激的影响因素分析

doi:10.16829/j.slxb.150765

兽类学报 ›› 2023, Vol. 43 ›› Issue (5): 479-488.DOI: 10.16829/j.slxb.150765

• 研究论文 • 下一篇

普氏原羚警戒行为和生理应激的影响因素分析

刘若爽¹, 石建斌¹, 刘定震², 沈心晨¹, 王庆庆¹, 徐雪飞¹, 郭冬生², 董世魁^1,3, 张毓⁴, 何玉邦⁵, 吴永林⁵

1 北京师范大学环境学院, 北京 100875;
2 北京师范大学生命科学学院, 生物多样性与生态工程教育部重点实验室, 北京 100875;
3 北京林业大学草业与草原学院, 北京 100083;
4 青海省林业和草原局, 西宁 810000;
5 青海湖国家级自然保护区管理局, 西宁 810007

收稿日期:2022-12-12 修回日期:2023-05-16 出版日期:2023-09-30 发布日期:2023-09-22
通讯作者: 石建斌,E-mail:jbshi@bnu.edu.cn
作者简介:刘若爽(1989-)，女，博士研究生，主要从事生理生态学研究.E-mail:201531180032@mailbox.bnu.edu.cn.
基金资助:
国家自然科学基金(31572281)；国家重大研发计划项目(2016YFC0501906)

Analysis of factors influencing vigilance and physiological stress in Przewalski’s gazelle

LIU Ruoshuang¹, SHI Jianbin¹, LIU Dingzhen², SHEN Xinchen¹, WANG Qingqing¹, XU Xuefei¹, GUO Dongsheng², DONG Shikui^1,3, ZHANG Yu⁴, HE Yubang⁵, WU Yonglin⁵

1 School of Environment, Beijing Normal University, Beijing 100875, China;
2 Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China;
3 School of Grassland Science, Beijing Forestry University, Beijing 100083, China;
4 Forestry and Grassland Bureau of Qinghai Province, Xining 810000, China;
5 Qinghai Lake National Nature Reserve Management Bureau, Xining 810007, China

Received:2022-12-12 Revised:2023-05-16 Online:2023-09-30 Published:2023-09-22

摘要/Abstract

摘要： 野生动物在面对自然胁迫(例如捕食者)和人为胁迫(例如道路交通)时，有可能产生能够影响动物个体健康和生存的生理和行为反应。升高糖皮质激素浓度和增强警戒行为是哺乳动物应对捕食风险时在生理和行为上最常见的两种反捕食响应。动物的反捕食策略权衡了对反捕食响应和其他生命活动的投入，以在个体生存和繁殖间寻求最大适合度。本研究以分布于青海湖流域部分区域的成年雌性普氏原羚(Procapra przewalskii)为研究对象，应用非损伤取样法采集其新鲜粪便样品，使用酶联免疫吸附测定法(ELISA)检测粪样中的皮质醇含量；结合焦点动物全事件取样法和瞬时扫描法进行行为取样，使用广义线性混合模型分析不同胁迫对雌性普氏原羚粪便糖皮质激素代谢物(FGMs)和警戒行为的影响。结果显示，在雌性普氏原羚野生种群中，FGMs和主要警戒行为指标在产羔期高于交配期，繁殖状态是影响FGMs和警戒行为的主要因素(F=39.162,P < 0.001)。与捕食者和草原围栏相比，公路和铁路交通对普氏原羚生理应激的影响更大(F=87.482,P < 0.001)，人类活动是导致雌性普氏原羚FGMs升高的重要因素。因此，日益增多的人为活动对野生动物造成的负面影响是未来保护工作中无法回避的挑战，如何在经济社会发展和野生动物保护的矛盾中寻求平衡，实现人与自然和谐发展，应引起决策者更多的重视。

关键词: 普氏原羚, 粪便糖皮质激素, 警戒行为, 人为胁迫

Abstract: Animals develop physiological and behavioral responses to cope with natural stressors (e. g., predators) or anthropogenic stressors (e. g., road traffic). However, these responses may affect the health and survival of individuals, leading to a range of serious wildlife conservation problems. Elevated glucocorticoid concentration and increased vigilance are two common responses to predation risk in mammals. Chronic high-level glucocorticoid concentration and vigilance occur at the expense of other life maintenance and reproduction activities, reflecting a trade-off between individual survival and future fecundity. In this study, a non-invasive sampling method was employed to collect fresh fecal samples from female Przewalski’s gazelles (Procapra przewalskii) and the cortisol concentrations in the samples were measured using ELISA. Focal-animal all-occurrence sampling and scan sampling of behavior were applied to collect data on the vigilance behaviour of female gazelles. Generalized linear mixed model was used to investigate the effects of different types of stressors on the fecal glucocorticoid metabolites (FGM) concentration and vigilance of female Przewalski’s gazelles. In wild Przewalski’s gazelle populations, reproductive status was the main factor influencing FGMs and vigilance (F = 39. 162, P < 0. 001), with higher FGMs and vigilance behavior in the lambing season than the rutting season. Anthropogenic stressors were important factors affecting FGMs of female Przewalski’s gazelles, with road and railway traffic contributing more to their physiological stress than natural predators and grassland fences (F = 87. 482, P < 0. 001). The negative impact of socio-economic development on wildlife is an inevitable challenge for Przewalski’s gazelle conservation. We should undertake great efforts to balance socio-economic development and wildlife conservation, and build a harmonious community for both humans and nature.

Key words: Przewalski’s gazelle (Procapra przewalskii), Fecal glucocorticoid metabolite (FGM), Vigilance, Anthropogenic stress

中图分类号:

Q958.12

刘若爽, 石建斌, 刘定震, 沈心晨, 王庆庆, 徐雪飞, 郭冬生, 董世魁, 张毓, 何玉邦, 吴永林. 普氏原羚警戒行为和生理应激的影响因素分析[J]. 兽类学报, 2023, 43(5): 479-488.

LIU Ruoshuang, SHI Jianbin, LIU Dingzhen, SHEN Xinchen, WANG Qingqing, XU Xuefei, GUO Dongsheng, DONG Shikui, ZHANG Yu, HE Yubang, WU Yonglin. Analysis of factors influencing vigilance and physiological stress in Przewalski’s gazelle[J]. ACTA THERIOLOGICA SINICA, 2023, 43(5): 479-488.

参考文献

Altmann J. 1973. Observational study of behavior:Sampling methods. Behaviour, 49:227-267.
Atickem A, Loe L E, Stenseth N C. 2014. Individual heterogeneity in use of human shields by mountain nyala. Ethology, 120 (7):715-725.
Beauchamp G. 2008. What is the magnitude of the group-size effect on vigilance? Behavioral Ecology, 19 (6):1361-1368.
Berger J. 2007. Fear, human shields and the redistribution of prey and predators in protected areas. Biology Letters, 3 (6):620-623.
Casagrande S, Garamszegi L Z, Goymann W, Donald J, Francis C D, Fuxjager M J, Husak J F, Johnson M A, Kircher B, Knapp R, Martin L B, Miller E T, Schoenle L A, Vitousek M N, Williams T D, Hau M. 2018. Do seasonal glucocorticoid changes depend on reproductive investment? A comparative approach in birds. Integrative and Comparative Biology, 58:739-750.
Chaves Ó, Fernandes F, Oliveira G, Bicca-Marques J C. 2019. Assessing the influence of biotic, abiotic, and social factors on the physiological stress of a large Neotropical primate in Atlantic forest fragments. Science of the Total Environment, 690:705-716.
Chen L W, Feng Z J, Cai P, Li Y B, Chen H J, Jiang Z G. 1997. Studies on the diurnal activities and time budgets of Przewalski's gazelle. Acta Theriologica Sinica, 17 (3):172-183. (in Chinese)
Childress M J, Lung M A. 2003. Predation risk, gender and the group size effect:Does elk vigilance depend upon the behaviour of conspecifics? Animal Behaviour, 66 (2):389-398.
Clinchy M, Sheriff M J, Zanette L Y. 2013. Predator-induced stress and the ecology of fear. Functional Ecology, 27 (1):56-65.
Creel S R, Fox J E, Hardy A, Sands J, Garrott B, Peterson R O. 2002. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conservation Biology, 16 (3):809-814.
Creel S R, Winnie J A, Christianson D D. 2009. Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. Proceedings of the National Academy of Sciences, 106 (30):12388-12393.
Crossin G T, Love O P, Cooke S J, Williams T D. 2016. Glucocorticoid manipulations in free-living animals:Considerations of dose delivery, life-history context and reproductive state. Functional Ecology, 30:116-125.
Darimont C T, Fox C H, Bryan H M, Reimchen T E. 2015. The unique ecology of human predators. Science, 349 (6250):858-860.
Dimond S, Lazarus J. 1974. Problem of vigilance in animal life. Brian Behavior and Evolution, 9 (1):60-79.
Ditmer M A, Rettler S J, Fieberg J R, Iaizzo P A, Laske T G, Noyce K V, Garshelis D L. 2018. American black bears perceive the risks of crossing roads. Behavioral Ecology, 29 (3):667-675.
Epps C W, Palsbøll P J, Wehausen J D, Roderick G K, Ramey R R, McCullough D R. 2005. Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecology Letters, 8 (10):1029-1038.
Fahrig L, Merriam G. 1994. Conservation of fragmented populations. Conservation Biology, 8 (1):50-59.
Fattorini N, Lovari S, Brunetti C, Baruzzi C, Cotza A, Macchi E, Pagliarella M C, Ferretti F. 2018. Age, seasonality, and correlates of aggression in female Apennine chamois. Behavioral Ecology & Sociobiology, 72:171.
Fattorini N, Ferretti F. 2019. To scan or not to scan? Occurrence of the group-size effect in a seasonally nongregarious forager. Ethology, 125:263-275.
Forman R T T, Alexander L E. 1998. Roads and their major ecological effects. Annual Review of Ecology and Systematics, 29 (1):207-231.
Gaynor K M, Cords M. 2012. Antipredator and social monitoring functions of vigilance behaviour in blue monkeys. Animal Behaviour, 84 (3):531-537.
Gerlach G, Musolf K. 2000. Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology, 14(4):1066-1074.
Girard-Buttoz C, Heistermann M, Rahmi E, Agil M, Fauzan P A, Engelhardt A. 2014. Costs of and investment in mate-guarding in wild long-tailed macaques (Macaca fascicularis):influences of female characteristics and male-female social bonds. International Journal of Primatology, 35 (3-4):701-724.
Goymann W. 2012. On the use of non-invasive hormone research in uncontrolled, natural environments:The problem with sex, diet, metabolic rate and the individual. Methods in Ecology and Evolution, 3 (4):757-765.
Hebblewhite M, White C A, Nietvelt C G, McKenzie J A, Hurd T E, Fryxell J M, Bayley S E, Paquet P C. 2005. Human activity mediates a trophic cascade caused by wolves. Ecology, 86 (8):2135-2144.
Hitchings S P, Beebee T J C. 1997. Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations:Implications for biodiversity conservation. Heredity, 79 (2):117-127.
Iglesias-Merchan C, Horcajada-Sánchez F, Diaz-Balteiro L, EscribanoAvila G, Lara-Romero C, Virgos E, Planillo A, Barja I. 2018. A new large-scale index (AcED) for assessing traffic noise disturbance on wildlife:stress response in a roe deer (Capreolus capreolus) population. Environmental Monitoring and Assessment, 190(4):185.
Jiang Z G, Feng Z J, Wang Z W, Chen L W, Cai P, Li Y B. 1995. Historical and currunt distributions of Przewalski's gazelles. Acta Theriologica Sinica, 15 (4):241-245. (in Chinese).
Keller I, Largiadèr C R. 2003. Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proceedings of the Royal Society B:Biological Sciences, 270 (1513):417-423.
Kuijper D P J, Bubnicki J W, Churski M, Mols B, van Hooft P. 2015. Context dependence of risk effects:Wolves and tree logs create patches of fear in an old-growth forest. Behavioral Ecology, 26(6):1558-1568.
Kumar V, Umapathy G. 2019. Non-invasive monitoring of steroid hormones in wildlife for conservation and management of endangered species-A review. Indian Journal Experimental Biology, 57:307-314.
Lazarus J, Symonds M. 1992. Contrasting effects of protective and obstructive cover on avian vigilance. Animal Behaviour, 43 (3):519-521.
Lei R H, Hu Z A, Jiang Z G, Yang W L. 2003. Phylogeography and genetic diversity of the critically endangered Przewalski's gazelle. Animal Conservation, 6 (4):361-367.
Li C W, Jiang Z G, Feng Z J, Yang X B, Yang J, Chen L W. 2009. Effects of highway traffic on diurnal activity of the critically endangered Przewalski's gazelle. Wildlife Research, 36 (5):379-385.
Li C L, Jiang Z G, Ping X G, Cai J, You Z Q, Li C W, Wu Y L. 2012a. Current status and conservation of the endangered Przewalski's gazelle Procapra przewalskii, endemic to the Qinghai-Tibetan Plateau, China. Oryx, 46 (1):145-153.
Li C L, Jiang Z G, Li L L, Li Z Q, Fang H X, Li C W, Beauchamp G. 2012b. Effects of reproductive status, social rank, sex and group size on vigilance patterns in Przewalski's gazelle. PLoS ONE, 7(2):7.
Li D Q, Jiang Z G, Wang Z W. 1999. Impacts of human activities on the distribution of the critically endangered Przewalski's gazelle.
Acta Ecologica Sinica, 19 (6):890-895. (in Chinese)
Li Z Q, Jiang Z G, Li C W. 2008. Dietary overlap of Przewalski's gazelle, Tibetan gazelle, and Tibetan sheep on the Qinghai-Tibet Plateau. Journal of Wildlife Management, 72 (4):944-948.
Li Z Q, Jiang Z G. 2008. Group size effect on vigilance:Evidence from Tibetan gazelle in upper Buha River, Qinghai-Tibet Plateau. Behavioural Processes, 78 (1):25-28.
Liang D N, Liu Y X, Ping X G, Jiang Z G, Li C W. 2021. Ensuring recovery for the Przewalski's gazelle. Science, 374:163.
Liu B W, Jiang Z G. 2002. Foraging strategy of Przewalski's gazelle(Procapra przewalskii). Acta Zoologica Sinica, 48 (3):309-316.(in Chinese)
Liu B W, Jiang Z G. 2003. Diet composition of wolves Canis lupus in the northeastern Qinghai-Tibet Plateau, China. Acta Theriologica, 48 (2):255-263.
Liu R, Shi J, Liu D, Dong S K, Zhang Y, Wu Y L, Guo D S. 2020. Effect of group size and reproductive status on faecal glucocorticoid concentration and vigilance in a free-ranging population of Przewalski's gazelle. Conservation Physiology, 8 (1):coaa027.
Lunde E T, Bech C, Fyumagwa R D, Jackson C R, Roskaft E. 2016. Assessing the effect of roads on impala (Aepyceros melampus) stress levels using faecal glucocorticoid metabolites. African Journal of Ecology, 54 (4):434-441.
McClure C J W, Ware H E, Carlisle J, Kaltenecker G, Barber J R. 2013. An experimental investigation into the effects of traffic noise on distributions of birds:Avoiding the phantom road. Proceedings of the Royal Society B:Biological Sciences, 280 (1773):20132290.
Millspaugh J J, Woods R J, Hunt K E, Raedeke K J, Brundige G C, Washburn B E, Wasser S K. 2001. Fecal glucocorticoid assays and the physiological stress response in elk. Wildlife Society Bulletin, 29 (3):899-907.
Nersesian C L, Banks P B, McArthur C. 2012. Behavioural responses to indirect and direct predator cues by a mammalian herbivore, the common brushtail possum. Behavioral Ecology and Sociobiology, 66 (1):47-55.
Palme R. 2019. Non-invasive measurement of glucocorticoids:Advances and problems. Physiology and Behavior, 199:229-243.
Parris K M, Velik-Lord M, North J M A. 2009. Frogs call at a higher pitch in traffic noise. Ecology and Society, 14 (1):25.
Pavitt A T, Pemberton J M, Kruuk L E B, Walling C A. 2016. Testosterone and cortisol concentrations vary with reproductive status in wild female red deer. Ecology and Evolution, 6:1163-1172.
Pecorella I, Fattorini N, Macchi E, Ferretti F. 2019. Sex/age differences in foraging, vigilance and alertness in a social herbivore. Acta Ethologica, 22:1-8.
Peng Y, He G J, Zhang Z M, Yin R Y. 2020. Landsat spectral index products over China. Science Data Bank. DOI:10. 11922/sciencedb. 986 2020-04-29
Romero L M, Dickens M J, Cyr N E. 2009. The reactive scope model-A new model integrating homeostasis, allostasis, and stress. Hormones and Behavior, 55:375-389.
Sapolsky R M, Romero L M, Munck A U. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1):55-89.
Sapolsky R M, Wingfield J C. 2003. Reproduction and resistance to stress:When and how. Journal of Neuroendocrinology, 15:711-724.
Saunders D A, Hobbs R J, Margules C R. 1991. Biological consequences of ecosystem fragmentation:A review. Conservation Biology, 5 (1):18-32.
Schwarzenberger F. 2007. The many uses of non-invasive faecal steroid monitoring in zoo and wildlife species. International Zoo Yearbook, 41 (1):52-74.
Scott K, Heistermann M, Cant M A, Vitikainen E I K. 2017. Group size and visitor numbers predict faecal glucocorticoid concentrations in zoo meerkats. Royal Society Open Science, 4:161017.
Selye H. 1936. A syndrome produced by diverse nocuous agents. Nature, 138:32.
Sheriff M J, Krebs C J, Boonstra R. 2010. The ghosts of predators past:Population cycles and the role of maternal programming under fluctuating predation risk. Ecology, 91 (10):2983-2994.
Sheriff M J, Dantzer B, Delehanty B, Palme R, Boonstra R. 2011. Measuring stress in wildlife:Techniques for quantifying glucocorticoids. Oecologia, 166:869-887.
Shi J B, Li D Q, Xiao W F. 2010. Influences of sex, group size, and spatial position on vigilance behavior of Przewalski's gazelles.
Acta Theriologica, 56 (1):73-79.
Ware H E, McClure C J W, Carlisle J D, Barber J R. 2015. A phantom road experiment reveals traffic noise is an invisible source of habitat degradation. Proceedings of the National Academy of Sciences of the United States of America, 112 (39):12105-12109.
Wasser S K, Bevis K, King G, Hanson E. 1997. Noninvasive physiological measures of disturbance in the northern spotted owl. Conservation Biology, 11 (4):1019-1022.
Wei W H, Jiang Y J, Zhu S W, Zhou W Y, Jiang Z G. 1998. Preliminarystudy on population sizes and affecting factors of Przewalski's gazelles (Procapra przewalskii). Acta Theriologica Sinica, 18(3):232-234. (in Chinese)
Wingfield J C. 2005. The concept of allostasis:coping with a capricious environment. Journal of Mammalogy, 86:248-254.
Xia C J, Xu W X, Yang W K, Blank D, Qiao J F, Liu W. 2011. Seasonal and sexual variation in vigilance behavior of Goitered gazelle (Gazella subgutturosa) in western China. Journal of Ethology, 29 (3):443-451.
Yang J, Jiang Z G, Zeng Y, Turghan M, Fang H X, Li C W. 2011. Effect of anthropogenic landscape features on population genetic differentiation of Przewalski's gazelle:main role of human settlement. PLoS ONE, 6 (5):e20144.
Yang J, Jiang Z G. 2011. Genetic diversity, population genetic structure and demographic history of Przewalski's gazelle (Procapra przewalskii):Implications for conservation. Conservation Genetics, 12 (6):1457-1468.
You Z Q, Jiang Z G. 2005. Courtship and mating behaviors in Przewalski's gazelle Procapra przewalskii. Acta Zoologica Sinica, 51(2):187-194. (in Chinese)
You Z Q, Jiang Z G, Li C. 2011. Location of rut stands vs. mating opportunities in Przewalski's gazelle:A field test of the 'Resource- Based Hypothesis' and 'Female Traffic Version of the Hotspot Hypothesis'. Current Zoology, 57 (6):701-708.
You Z Q, Jiang Z G, Li C W, Mallon D. 2013. Impacts of grassland fence on the behavior and habitat area of the critically endangered Przewalski's gazelle around the Qinghai Lake. Chinese Science Bulletin, 58 (18):2262-2268.
Zbyryt A, Bubnicki J W, Kuijper D P J, Dehnhard M, Churski M, Schmidt K. 2018. Do wild ungulates experience higher stress with humans than with large carnivores? Behavioral Ecology, 29(1):19-30.
Zhang L, Liu J Z, Wang D J, Schaller G B, Wu Y L, Harris R B, Zhang K J, Lu Z. 2013. Distribution and population status of Przewalski's gazelle, Procapra przewalskii (Cetartiodactyla, Bovidae). Mammalia, 77 (1):31-40.
Zhang L, Liu J, McShea W J, Wu Y L, Wang D J, Lu Z. 2014. The impact of fencing on the distribution of Przewalski's gazelle. Journal of Wildlife Management, 78 (2):255-263.
刘丙万, 蒋志刚. 2002. 普氏原羚的采食对策. 兽类学报, 48 (3):309-316.
李江宁. 2021. 青海:世界极度濒危物种普氏原羚 14 年种群数量增约 9 倍. 中国新闻网. http://www.chinanews.com/sh/2021/04-01/9445751.shtml (2021-10-17)
李迪强, 蒋志刚, 王祖望. 1999. 人类活动对普氏原羚分布的影响.生态学报, 19 (6):890-895.
陈立伟, 冯祚建, 蔡平, 李永波, 陈洪舰, 蒋志刚. 1997. 普氏原羚昼间行为时间分配的研究. 兽类学报, 17 (3):172-183.
彭燕, 何国金, 张兆明, 尹然宇. 2020. 中国区域 Landsat 遥感指数产品. Science Data Bank. DOI:10. 11922/sciencedb.986 2020-04-29
蒋志刚, 冯祚建, 王祖望, 陈立伟, 蔡平, 李永波. 1995. 普氏原羚的历史分布与现状. 兽类学报, 15 (4):241-245.
魏万红, 姜永进, 朱申武, 周文扬, 蒋志刚. 1998. 普氏原羚种群大小及影响因素的初步研究. 兽类学报, 18 (3):232-234.

[1]	尤文远石建斌路飞英董世魁李晓文张子慧. 普氏原羚集群的群体决策过程[J]. , 2013, 33(4): 293-299.
[2]	于道平, 蒋文华, 韩德民. 长江江豚对人工投食适应过程的观察[J]. , 2007, 27(4): 365-369.
[3]	叶润蓉, 蔡平, 彭敏, 卢学峰, 马世震. 普氏原羚的分布和种群数量调查[J]. , 2006, 26(4): 373-379.
[4]	刘丙万　蒋志刚. 普氏原羚生境选择的数量化分析[J]. , 2002, 22(1): 15-21.
[5]	李迪强，蒋志刚，王祖望. 普氏原羚的活动规律与生境选择[J]. , 1999, 19(1): 17-24.
[6]	魏万红，姜永进,朱申武,周文扬,蒋志刚. 普氏原羚种群大小及影响因素的初步研究[J]. , 1998, 18(3): 232-234.
[7]	陈立伟　冯祚建蔡　平　李永波　陈洪舰. 普氏原羚昼间行为时间分配的研究[J]. , 1997, 17(3): 172-183.
[8]	蒋志刚，冯祚建，王祖望，陈立伟. 普氏原羚的历史分布与现状[J]. , 1995, 15(4): 241-245.

普氏原羚警戒行为和生理应激的影响因素分析

Analysis of factors influencing vigilance and physiological stress in Przewalski’s gazelle

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