Feeding behavior of sympatric rodents in the Alxa Desert in response to different grazing patterns

doi:10.16829/j.slxb.150800

Abstract

Abstract: The fragile ecosystem of the Alxa Desert is sensitive to human disturbance and different grazing patterns lead to different vegetation resource types, density, distribution, coverage, substrate and animal perception of predation risk. The feeding differences of desert sympatric rodents under different grazing disturbances are of great significance for the maintenance of biodiversity in desert areas. In 2020, infrared camera trap technology was used to observe the feeding behavior of three dominant rodent species, namely Dipus sagitta, Orientallactaga sibirica, and Meriones meridianus, which coexisted in the same area in the Alax Desert. The results showed that: (1) the population density of the dominant rodent species was positively related to their feeding behavior under different grazing patterns. Grazing increased O. sibirica population density, and its feeding behavior also accounted for more in grazing-intensive habitats. M. meridianus had higher population density and more feeding behavior in habitats with low grazing intensity and high vegetation coverage. D. sagitta devoted more foraging effort in more grazing-intensive habitats. (2) Under the same grazing mode, M. meridianus adopted a combined feeding strategy of ‘foraging + feeding + storage’ , while D. sagitta and O. sibirica adopted the feeding strategy of ‘foraging + feeding’ . These results indicated that the feeding behaviors of rodent species with various feeding strategies were affected by grazing patterns according to changing environmental factors such as rodent population density, habitat vegetation, and soil.

Key words: Desert, Rodents, Coexistence, Feeding behavior, Infrared camera

摘要： 阿拉善荒漠脆弱生态系统对人为干扰反应较敏感，不同放牧方式导致该生态系统的植被资源类型、密度、分布、盖度、基质以及动物感知捕食风险等各不相同。同域分布的荒漠啮齿动物在不同干扰下的觅食差异性对于荒漠地区生物多样性的维持具有重要意义。本文于2020年通过红外相机陷阱技术对阿拉善荒漠区同域共存的三趾跳鼠(Dipus sagitta)、五趾跳鼠(Orientallactaga sibirica)和子午沙鼠(Meriones meridianus)3种优势鼠种在3种不同放牧方式下的摄食行为进行观测，结果显示：(1)不同放牧方式下3种啮齿动物优势种的种群密度与摄食行为成正比，放牧增加了五趾跳鼠种群密度，其摄食行为也在放牧强度大的生境中占比更多；子午沙鼠在放牧强度较小且植被盖度较高的生境中种群密度较高，摄食行为也多集中于此；三趾跳鼠在不同放牧方式下种群密度差异不大，相对来说在放牧强度更大的生境中花费的觅食努力更大；(2)相同放牧方式下，子午沙鼠面对食物会采取“觅食+取食+贮食”相结合的摄食策略，而三趾跳鼠和五趾跳鼠更倾向于“觅食+原地取食”的摄食策略。由此表明，尽管不同鼠种具有差异化的摄食策略，但是它们的觅食行为会受到放牧方式的影响，而这种影响是通过改变啮齿动物种群密度、栖息地植被和土壤特征等环境因子造成的。

关键词: 荒漠, 啮齿动物, 同域共存, 摄食行为, 红外相机

CLC Number:

Q958.1

LIU Lina, YUAN Shuai, LI Xin, FU Heping, WU Xiaodong. Feeding behavior of sympatric rodents in the Alxa Desert in response to different grazing patterns[J]. ACTA THERIOLOGICA SINICA, 2023, 43(6): 689-701.

刘丽娜, 袁帅, 李鑫, 付和平, 武晓东. 阿拉善荒漠啮齿动物优势种觅食活动对不同放牧方式的响应[J]. 兽类学报, 2023, 43(6): 689-701.

References

Baker M A A, Brown J S. 2010. Islands of fear: effects of wooded patches on habitat suitability of the striped mouse in a South African grassland. Functional Ecology, 24 (6): 1313-1322.
Bejder L, Samuels A, Whitehead H, Finn H, Allen S J. 2009. Impact assessment research: use and misuse of habituation, sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli. Marine Ecology Progress Series, 395: 177-185.
Boake C R B. 1998. Handbook of ethological methods. The Quarterly Review of Biology, 73 (2): 248-252.
Brown J S, Kotler B P, Mitchell W A. 1994. Foraging theory, patch use, and the structure of a Negev Desert Granivore Community. Ecology, 75 (8): 2286-2300.
Caruso N, Lucherini M, Fortin D, Casanave E B. 2016. Speciesspecific responses of carnivores to human-induced landscape changes in central argentina. PLoS ONE, 11 (3): e0150488.
Che Y, Li Z Q. Vigilance behavior of animals: overview and perspective. Sichuan Journal of Zoology, 33 (1): 144-150. (in Chinese)
Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13 (8): 1194-1202.
Chen L D, Fu B J. 2000. Ecological significance, characteristics and types of disturbance. Acta Ecologica Sinica, 20 (4): 581-586. (in Chinese)
Crego R D, Jiménez J E, Rozzi R. 2018. Macroand micro-habitat selection of small rodents and their predation risk perception under a novel invasive predator at the southern end of the Americas. Mammal Research, 63 (3): 9-10.
Dilana·Ailiken, Aergen·Hadier, Dai K. 2010. Study on characteristics of mictohabitat selection and feeding behavior of Meriones meridianus. Journal of Arid Land Resources and Environment, 24 (8): 186-189. (in Chinese)
Falcy M R, Danielson B J. 2013. A complex relationship between moonlight and temperature on the foraging behavior of the Alabama beach mouse. Ecology, 94 (11): 2632-2637.
Fan Y G. 2020. Effects of changes in food resources on habitat selection and foraging behavior of greater white fronted goose wintering at Shengjin Lake. Master thesis. Hefei: Anhui University. (in Chinese)
Ferrer-i-Cancho R, Hernández-Fernández A, Lusseau D, Agoramoorthy G, Hsu M J, Semple S. 2013. Compression as a universal principle of animal behavior. Cognitive Science, 37 (8): 1565-1578.
Flowerdew J R, Shore R F, Poulton S M C, Sparks T H. 2004. Live trapping to monitor small mammals in Britain. Mammal Review, 34 (1-2): 31-50.
Frafjord K. 2016. Influence of reproductive status: home range size in water voles (Arvicola amphibius). PLoS ONE, 11 (4): e0154338.
Fu H P, Yang Z L, Wu X D, Narisu. 2007. The pattern of desert rodent community under different disturrbance and scales. Journal of Inner Mongolia Agricultural University (Natural Science Edition), 28 (1): 51-56. (in Chinese)
Gan H J, Zhang R, Ma J, Zhao Y H, Zhao Y Q, Li W, Su B, Su J L, Yuan S, Fu H P. 2021. Population age structure and seasonal dynamics of two jerboa species in different habitats in Alxa Desert area. Grassland and Prataculture, 33 (4): 32-35, 53. (in Chinese)
Gaynor K M, Hojnowski C E, Carter N H, Brashares J S. 2018. The influence of human disturbance on wildlife nocturnality. Science, 360 (6394): 1232-1235.
Hodgkison R, Ayasse M, Häberlein C, berlein C, Schulz S, Zubaid A, Mustapha W A W, Kunz T H, Kalko E K V. 2013. Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the new and old world tropics. Functional Ecology, 27 (4): 1075-1084.
HooPer D U, Vitousek P M. 1997. The effects of plant composition and diversity on ecosystem processes. Science, 277 (5330): 1302-1305.
Jiang G Q. 2011. Effect of seed size, shape and tannin content on seed fate and dispersal of artificial seeds. Master thesis. Luoyang:Henan University of Science and Technology. (in Chinese)
Knight R L, Fitzner R E. 1985. Human disturbance and nest site placement in black-billed magpies. Journal of Field Ornithology, 56 (2): 153-157.
Lang Z W, Gong H D. 2016. Foraging behavior of scatter-hoarding rodent in subtropical and tropical forests. Journal of West China Forestry Science, 45 (6): 133-141. (in Chinese)
Li J S, Song Y L, Wang X Z, Zeng Z G. 2005. Spatial pattern of small mammals community diversity in different grazing pressure in montane desert-steppe. Acta Ecologica Sinica, 25 (1): 51-58.(in Chinese)
Li X, Yuan S, Fu H P, Wu X D, Yang S W, Ji Y, Liu J W, Xu H, Narisu, Yuan W, Zhang Z R. 2020. Activity rhythm and influencing factors of two dominant rodent species in desert region. Acta Theriologica Sinica, 40 (6): 585-594. (in Chinese)
Lin T J. 2022. Effects of temperature, humidity and rainfall on rodent activity rhythm in a subtropical evergreen broad-leaved forest in Ailao Mountain. Master thesis. Hefei: Anhui University. (in Chinese)
Liu X H, Wu P F, Songer M, Cai Q, He X B, Zhu Y, Shao X M. 2013. Monitoring wildlife abundance and diversity with infra-red camera traps in Guanyinshan Nature Reserve of Shaanxi Province, China. Ecological Indicators, 33: 121-128.
Loggins A A, Shrader A M, Monadjem A, McCleery R A. 2019. Shrub cover homogenizes small mammals’activity and perceived predation risk. Scientific Reports, 9 (1): 16857.
Mohr K, Vibe-Petersen S, Jeppesen L L, Bildsøe M, Leirs H. 2003. Foraging of multimammate mice, Mastomys natalensis, under different predation pressure: cover, patch-dependent decisions and density-dependent GUDs. Oikos, 100 (3): 459-468.
Mori E, Ferretti F, Fattorini N. 2019. Alien war: ectoparasite load, diet and temporal niche partitioning in a multi-species assembly of small rodents. Biological Invasions, 21 (11): 3305-3318.
Narisu, Su H, Wu X D. 2009. Botanic food preference of Allactaga sibirica forster and its relationship with the vegetation conditions of their habitat. Acta Agrestia Sinica, 17 (3): 383-388. (in Chinese)
Schradin C, Schmohl G, Rödel H G, Schoepf I, Treffler S M, Brenner J, Bleeker M, Schubert M, König B, Pillay N. 2010. Female home range size is regulated by resource distribution and intraspecific competition: A long-term field study. Animal Behaviour, 79(1): 195-203.
Sévêque A, Gentle L K, Vicente LóPez‐Bao J, Yarnell R W, Uzal A. 2021. Impact of human disturbance on temporal partitioning within carnivore communities. Mammal Review, 52 (1): 67-81.
Shuai L Y, Song Y L. 2011. Foraging behavior of the midday gerbil(Meriones meridianus): combined effects of distance and microhabitat. Behavioural Processes, 86 (1): 143-148.
Soto-Shoender J R, McCleery R A, Monadjem A, Gwinn D C. 2018. The importance of grass cover for mammalian diversity and habitat associations in a bush encroached savanna. Biological Conservation, 221: 127-136.
Symes C T, Wilson J W, Woodborne S M, Shaikh Z S, Scantlebury M M G. 2013. Resource partitioning of sympatric small mammals in an African forest-grassland vegetation mosaic. Austral Ecology, 38: 721-729.
Viviano A, Scarfò M, Mori E. 2022. Temporal partitioning between forest-dwelling small rodents in a mediterranean deciduous woodland. Animals (Basel), 12 (3): 279.
Wang B, Ye C X, Cannon C H, Chen J. 2013. Dissecting the decision making process of scatter-hoarding rodents. Oikos, 122 (7):1027-1034.
Wang T T, Baimaciren, Hai S Z, Wang D. 2015. Construction for the ethogram of Brandt’ s voles (Lasiopodomys brandtii). Acta Agrestia Sinica, 23 (3): 646-652. (in Chinese)
Wang Y F, Wang S P. 1999. Influence of different stocking rates on aboveground present biomass and herbage quality in Inner Mongolia steppe. Acta Prataculturae Sinica, 8 (1): 15-20. (in Chinese)
Wu X D, Yuan S, Fu H P, Zhang X D, Zhang F S, Gao Q R. 2016. Responses of dominant rodentspecies to climate change in different disturbed habitats in the Alashan Desert. Acta Ecologica Sinica, 36 (6): 1765-1773. (in Chinese)
Yang S W. 2021. Response mechanism of rodent metacommunity in desert area to disturbance and climate change. Ph. D thesis. Hohhot: Inner Mongolia Agricultural University. (in Chinese)
Yuan S, Li X, Hou S J, Yang S W, Yue X X, Zhang Z R, Fu H P, Wu X D. 2021. Estimating the population density of desert rodents using a camera trap method. Pratacultural Science, 38 (3): 571-579. (in Chinese)
Yuan S, Yang S W, Fu H P, Li Y N, Wu X D, Yue X X. 2017. The effect of successive grazing on the home range of northern three toed jerboa (Dipus sagitta) in Alax Desert. Chinese Journal of Zoology, 52 (6): 964-972. (in Chinese)
Zhang C J. 2022. Study on the feeding habits of three rodents in Gannan grassland under different disturbance habitats. Master thesis. Lanzhou: Gansu Agricultural University. (in Chinese)
Zhang C M, Zhi Y J, Lu P, Shao M Q, Dai N H. 2000. Energy expenditure and foraging behavior of wintering Tundra Swan and Swan Goose in alotus pond reclamation area in Poyang Lake. Chinese Journal of Ecology, 38 (3): 785-790. (in Chinese)
Zhao T B, Zhang Z B, Li X M, Zhang C F, Wu J P, Qi L. 2001. The population nichei of Rhombomys opimus and Meriones meridian. Acta Theriologica Sinica, 21 (1): 76-79. (in Chinese)
Zhao Y L, Wang S Y, Duan C C, Jiang W X, Xu Z G. 2018. Behavioral rhythm of captive Chrysolophus amherstiae in summer and autumn. Chinese Journal of Ecology, 37 (10): 2995-3000. (in Chinese)
王艳芬, 汪诗平. 1999. 不同放牧率对内蒙古典型草原牧草地上现存量和净初级生产力及品质的影响. 草业学报, 8 (1): 15-20.
王涛涛, 白玛次仁, 海淑珍, 王登. 2015. 布氏田鼠行为谱的构建. 草地学报, 23 (3): 646-652.
车烨, 李忠秋. 2014. 动物的警戒行为: 回顾及展望. 四川动物, 33(1): 144-150.
甘红军, 张蓉, 马久, 赵云华, 赵永泉, 李伟, 苏巴特尔, 苏佳楼, 袁帅, 付和平. 2021. 阿拉善荒漠区两种跳鼠种群年龄结构及其季节动态特征. 草原与草业, 33 (4): 32-35, 53.
付和平, 杨泽龙, 武晓东, 那日苏. 2007. 不同干扰和尺度下荒漠啮齿动物群落格局. 内蒙古农业大学学报 (自然科学版), 28 (1):51-56.
地拉娜·艾力肯, 阿尔根·哈地尔, 戴昆. 2010. 子午沙鼠的微栖息地选择特征及其对采食行为研究. 干旱区资源与环境, 24 (8):186-189.
刘焕金, 冯敬义, 李承节, 石永刚, 杨贵增, 陈子敬, 王根录. 1984. 子午沙鼠生态的调查研究. 动物学杂志, 4 (8): 21-25.
李俊生, 宋延龄, 王学志, 曾治高. 2005. 放牧压力条件下荒漠草原小型哺乳动物群落多样性的空间格局. 生态学报, 25 (1):51-58.
李鑫, 袁帅, 付和平, 武晓东, 杨素文, 纪羽, 刘建文, 旭花, 那日苏, 袁伟, 张卓然. 2020. 荒漠区两种优势鼠种的活动节律及其影响因子. 兽类学报, 40 (6): 585-594.
杨素文. 2021. 荒漠区啮齿动物集合群落对人为干扰及气候变化的响应机制. 呼和浩特: 内蒙古农业大学博士学位论文.
张彩军. 2022. 不同干扰生境下甘南草原三种啮齿动物的食性研究. 兰州: 甘肃农业大学硕士学位论文.
张聪敏, 植毅进, 卢萍, 邵明勤, 戴年华. 2019. 鄱阳湖藕田越冬期小天鹅和鸿雁能量支出与取食行为比较. 生态学杂志, 38 (3):785-790.
陈利顶, 傅伯杰. 2000. 干扰的类型、特征及其生态学意义. 生态学报, 20 (4): 581-586.
武晓东, 袁帅, 付和平, 张晓东, 张福顺, 高全荣. 2016. 不同干扰下阿拉善荒漠啮齿动物优势种对气候变化的响应. 生态学报, 36(6): 1765-1773.
范言广. 2020. 食物资源变化对升金湖越冬白额雁生境选择和觅食行为的影响. 合肥: 安徽大学硕士学位论文.
林天杰. 2022. 温度、湿度和降雨对哀牢山亚热带常绿阔叶林内啮齿动物活动节律的影响. 合肥: 安徽大学硕士学位论文.
尚玉昌. 2006. 动物的行为节律. 生物学通报, 41 (10): 8-10.
郎政伟, 巩合德. 2016. 亚热带和热带森林内小型啮齿动物觅食行为差异. 西部林业科学, 45 (6): 133-141.
赵天飙, 张忠兵, 李新民, 张春福, 邬建平, 齐林. 2001. 大沙鼠和子午沙鼠的种群生态位. 兽类学报, 21 (1): 76-79.
赵运林, 王双业, 段酬苍, 姜卫星, 徐正刚. 2018. 笼养白腹锦鸡(Chrysolophus amherstiae) 夏、秋季行为节律. 生态学杂志, 37(10): 2995-3000.
赵肯堂. 1964. 三趾跳鼠 (Dipus sagitta Pallas) 的生态研究. 动物学杂志, 2 (5): 59-62.
娜日苏, 苏和, 武晓东. 2009. 五趾跳鼠的植物性食物选择与其栖息地植被的关系. 草地学报, 17 (3): 383-388.
袁帅, 李鑫, 侯帅君, 杨素文, 岳秀贤, 张卓然, 付和平, 武晓东. 2021. 应用红外相机陷阱法估计荒漠啮齿动物种群密度. 草业科学, 38 (3): 571-579.
袁帅, 杨素文, 付和平, 李燕妮, 武晓东, 岳秀贤. 2017. 阿拉善荒漠连续放牧对三趾跳鼠巢区的影响. 动物学杂志, 52 (6):964-972.
梁杰荣, 肖运峰. 1982. 五趾跳鼠的一些生态资料. 动物学杂志, 4(10): 24-25.
焦广强. 2011. 大小、形状及单宁含量对人工种子扩散和命运的影响. 洛阳: 河南科技大学硕士学位论文.
戴昆, 姚军, 胡德夫. 1998. 准噶尔盆地南缘荒漠鼠类的微栖息地选择. 干旱区研究, 15 (3): 34-37.

[1]	ZHANG Rumei, ZHANG Qing, YANG Xiao, ZHANG Farui, ZHAO Ding, PANG Dehong, YANG Kong, GUAN Tianpei. Spatial and temporal distribution patterns of mammal diversity in alpine ecosystems: a case study in Xuebaoding area of Giant Panda National Park [J]. ACTA THERIOLOGICA SINICA, 2023, 43(5): 533-543.
[2]	SONG Yuhao, BI Junhuai, Wensuyaletu, WANG Guolin, LI Feng, Lü Wenbing, ZHOU Yifan, PAN Xingxing, ZHANG Ruidong. Group behavior and seasonal changes of Capra sibirica in Urad Desert, Inner Mongolia [J]. ACTA THERIOLOGICA SINICA, 2023, 43(5): 544-552.
[3]	Qiwei WANG, Hengyue ZHAO, Qin LIU, Neng WAN, Zhibing ZHU, Hongyu NIU, Hongmao ZHANG. Mammal diversity in the forest fragments of Wuhan City [J]. ACTA THERIOLOGICA SINICA, 2023, 43(3): 258-269.
[4]	XIE Peigen, HU Juan, LI Tingting, GUO Rui, XU Lijuan, SONG Xiao, LI Jiaqi, XU Aichun. Distribution and activity patterns of wild boar (Sus scrofa) in the Qingliangfeng National Nature Reserve, Zhejiang Province [J]. ACTA THERIOLOGICA SINICA, 2022, 42(2): 168-176.
[5]	ZHU Yunlong, YANG Xifu, GU Haifeng, TENG Yuwei, ZHANG Zhibin. Effects of seed coat thickness on rodents' seed dispersal behavior and seed fate [J]. ACTA THERIOLOGICA SINICA, 2021, 41(6): 667-675.
[6]	SHAO Ruiqing, LI Yankuo, ZHONG Yifeng, WU Heping, LUO Xiaomin, XIONG Yu, CAO Kaiqiang. Preliminary survey on mammal and bird species diversity using infrared camera traps in the Matoushan National Nature Reserve, Jiangxi Province [J]. ACTA THERIOLOGICA SINICA, 2021, 41(6): 706-713.
[7]	LI Yuan, SHEN Youbi, WANG Minghui, YI Xianfeng, WANG Zhenyu. Seed-hoarding preferences of rodents for cork oak(Quercus variabilis) and Henry's chestnut(Castanea henryi): testing the high-tannin hypothesis [J]. ACTA THERIOLOGICA SINICA, 2021, 41(3): 338-343.
[8]	MA Duifang, SUN Zhangyun, HU Dazhi, AN Bei, CHEN Liuyang, ZHANG Dexi, DONG Kai, ZHANG Lixun. Camera-trapping survey of the mammal diversity in the Qilian Mountains National Nature Reserve, Gansu Province [J]. ACTA Theriologica Sinica, 2021, 41(1): 90-98.
[9]	LI Xin, YUAN Shuai, FU Heping, WU Xiaodong, YANG Suwen, JI Yu, LIU Jianwen, XU Hua, Narisu, Yuan Wei, Zhang Zhuoran. Activity rhythm and influencing factors of two dominant rodents species in desert region [J]. ACTA THERIOLOGICA SINICA, 2020, 40(6): 585-594.
[10]	LIU Bangyou, ZHANG Tingyue, LIANG Sheng, BAI Xiaojie, LIU Wei. Comparison of birds’ and mammals’ diversities using camera-trapping survey in Guizhou Chishui Alsophila National Nature Reserve and its surrounding areas [J]. ACTA THERIOLOGICA SINICA, 2020, 40(5): 503-519.
[11]	DUAN Xiaomin, LIU Jia, LIN Jianzhong, LI Jiaqi, ZHOU Qihai. Preliminary investigation on mammals and birds using infrared cameras in Chongzuo White-Headed Langur Nature Reserve, Guangxi [J]. ACTA THERIOLOGICA SINICA, 2020, 40(4): 380-389.
[12]	HOU Xiang, ZHANG Bo, HAN Ning, FENG Tuo, WANG Jing, CHEN Xiaoning, CHANG Gang. Differences in feeding and hoarding behaviors between intact and weevil-infested seeds of Quercus aliena var. acuteserrata by Apodemus draco and Niviventer confucianus under enclosure conditions [J]. ACTA THERIOLOGICA SINICA, 2020, 40(4): 390-397.
[13]	LI Jianliang, LI Jiaqi, WANG Liang, PEI Pengzu, MA Donghui, ZHUO Mengya, BAO Xinkang. The analysis on activity rhythms of several ungulates in extreme arid desert region based on infrared camera data [J]. ACTA THERIOLOGICA SINICA, 2020, 40(2): 120-128.
[14]	GUO Rui, XU Lijuan, WANG Xuchi, LIU Wei, FAN Penglai, XU Aichun. Preliminary investigation on mammal and bird resources using infrared camera traps in Qianqingtang Area of Zhejiang Qingliangfeng National Nature Reserve [J]. ACTA THERIOLOGICA SINICA, 2020, 40(2): 183-192.
[15]	WANG Cheng, SU Haijun, HU Canshi, SHI Lei, ZHANG Mingming. Spatial distribution of sympatric Rhinopithecus brelichi and Macaca thibetana in Fanjingshan National Nature Reserve, Guizhou, China [J]. ACTA THERIOLOGICA SINICA, 2020, 40(2): 193-200.