, Volume 180, Issue 1, pp 149–159 | Cite as

Successive sheep grazing reduces population density of Brandt’s voles in steppe grassland by altering food resources: a large manipulative experiment

  • Guoliang Li
  • Baofa Yin
  • Xinrong Wan
  • Wanhong Wei
  • Guiming Wang
  • Charles J. Krebs
  • Zhibin ZhangEmail author
Population ecology - Original research


Livestock grazing has shaped grassland ecosystems around the world. Previous studies indicated grazing showed various impacts on small rodents; however, most studies were conducted over 1–2 years without controlling for confounding factors such as immigration/emigration and predation in rodents. Brandt’s voles (Lasiopodomys brandtii) are generally recognized as pests because of food overlap with domestic herbivores, but are also important for biodiversity conservation because they provide nests or food to many birds. Fully understanding the ecological relationship between domestic herbivores and small mammals is essential to making ecosystem management decisions. To address these needs, we carried out a field experiment during the period 2010–2013 to assess the effects of sheep grazing on vegetation and the population density of Brandt’s voles along a gradient of three grazing intensities by using 12 large-scale enclosures. Responses of Brandt’s voles to livestock grazing varied with grazing intensity and year. As compared to the control group, sheep grazing had no effect on vole abundance in the first year but an overall negative effect on vole abundance in the following 3 years. Successive grazing caused decreases in survival and male body mass of voles, but had no significant effect on fecundity. Negative effects of grazing were associated with a grazing-induced deterioration in both food quantity (reflected by biomass and cover of less-preferred plants), and food quality (measured by tannin and total phenol content). Our findings highlight the urgent need for more flexible management of yearly rotational grazing to optimize livestock production while maintaining species diversity and ecosystem health.


Biodiversity loss Food quality Food quantity Pest management Rotational grazing 



We thank the Maodeng Pasture of Xilinhot City and the Grassland Station of Xilingol League for their kind help in our field experiments. We thank all the students and volunteers involved in the field work. We are grateful to Prof. Marcel Holyoak of the University of California Davis for his valuable assistance and comments on this manuscript. This study was supported by the State Basic Research Program of the Ministry of Science and Technology (2007CB109100) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11050000).

Author contribution statement

Z. Z. designed the experiments. G. L., B. Y., X. W. and W. W. performed the experiments. G. L. analyzed the data. G. L. and Z. Z. wrote the manuscript; G. W. and C. J. K. contributed to the data analysis and manuscript writing.

Supplementary material

442_2015_3455_MOESM1_ESM.pdf (296 kb)
Supplementary material 1 (PDF 296 kb)


  1. Anderson DR, Burnham KP, Gould WR, Cherry S (2001) Concerns about finding effects that are actually spurious. Wildlife Soc B 29:311–316Google Scholar
  2. Arsenault R, Owen-Smith N (2002) Facilitation versus competition in grazing herbivore assemblages. Oikos 97:313–318. doi: 10.1034/j.1600-0706.2002.970301.x CrossRefGoogle Scholar
  3. Augustine DJ, Springer TL (2013) Competition and facilitation between a native and a domestic herbivore: trade-offs between forage quantity and quality. Ecol Appl 23:850–863PubMedCrossRefGoogle Scholar
  4. Bryant JP, Wieland GD, Clausen T, Kuropat P (1985) Interactions of snowshoe hare and feltleaf willow in Alaska. Ecology 66:1564–1573. doi: 10.2307/1938018 CrossRefGoogle Scholar
  5. Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information theoretic approach. Springer, New YorkGoogle Scholar
  6. Davidson AD et al (2010) Rapid response of a grassland ecosystem to an experimental manipulation of a keystone rodent and domestic livestock. Ecology 91:3189–3200. doi: 10.1890/09-1277.1 PubMedCrossRefGoogle Scholar
  7. Davidson AD, Detling JK, Brown JH (2012) Ecological roles and conservation challenges of social, burrowing, herbivorous mammals in the world’s grasslands. Front Ecol Environ 10:477–486. doi: 10.1890/110054 CrossRefGoogle Scholar
  8. Diaz S et al (2007) Plant trait responses to grazing—a global synthesis. Global Change Biol 13:313–341. doi: 10.1111/j.1365-2486.2006.01288.x CrossRefGoogle Scholar
  9. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406. doi: 10.1126/science.1251817 PubMedCrossRefGoogle Scholar
  10. Evans DM, Villar N, Littlewood N, Pakeman R, Evans S, Dennis P, Skartveit J, Redpath S (2015) The cascading impacts of livestock grazing in upland ecosystems: a 10 year experiment. Ecosphere. doi: 10.1890/ES14-00316.1 Google Scholar
  11. Foster CN, Barton PS, Lindenmayer DB (2014) Effects of large native herbivores on other animals. J Appl Ecol 51:929–938. doi: 10.1111/1365-2664.12268 CrossRefGoogle Scholar
  12. Gill RB, Carpenter LH, Bartmann RM, Baker DL, Schoonveld GG (1983) Fecal analysis to estimate mule deer diets. J Wildlife Manage 47:902–915. doi: 10.2307/3808149 CrossRefGoogle Scholar
  13. Golluscio RA, Austin AT, Martinez GCG, Gonzalez-Polo M, Sala OE, Jackson RB (2009) Sheep grazing decreases organic carbon and nitrogen pools in the Patagonian Steppe: combination of direct and indirect effects. Ecosystems 12:686–697. doi: 10.1007/s10021-009-9252-6 CrossRefGoogle Scholar
  14. Gustafson G, Ryan CA (1976) Specificity of protein turnover in tomato leaves: accumulation of proteinase-inhibitors, induced with wound hormone, Piif. J Biol Chem 251:7004–7010PubMedGoogle Scholar
  15. Haapakoski M, Sundell J, Ylonen H (2012) Predation risk and food: opposite effects on overwintering survival and onset of breeding in a boreal rodent. J Anim Ecol 81:1183–1192. doi: 10.1111/j.1365-2656.2012.02005.x PubMedCrossRefGoogle Scholar
  16. Hilborn R, Redfield JA, Krebs CJ (1976) Reliability of enumeration for mark and recapture census of voles. Can J Zool 54:1019–1024. doi: 10.1139/Z76-114 CrossRefGoogle Scholar
  17. Jiang G et al (2011) Effects of ENSO-linked clilmate and vegetation on population dynamics of sympatric rodent species in semiarid grasslands of Inner Mongolia, China. Can J Zool 89:678–691. doi: 10.1139/Z11-048 CrossRefGoogle Scholar
  18. Karels TJ, Byrom AE, Boonstra R, Krebs CJ (2000) The interactive effects of food and predators on reproduction and overwinter survival of arctic ground squirrels. J Anim Ecol 69:235–247. doi: 10.1046/j.1365-2656.2000.00387.x CrossRefGoogle Scholar
  19. Krebs CJ (1966) Demographic changes in fluctuating populations of Microtus californicus. Ecol Monogr 36:240–273CrossRefGoogle Scholar
  20. Krebs CJ (2014) Rodent biology and management. Integr Zool 9:229–230. doi: 10.1111/1749-4877.12090 PubMedCrossRefGoogle Scholar
  21. Krebs CJ (2015) One hundred years of population ecology: successes, failures and the road ahead. Integr Zool 10:233–240. doi: 10.1111/1749-4877.12130 PubMedCrossRefGoogle Scholar
  22. Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118. doi: 10.2307/2937171 CrossRefGoogle Scholar
  23. Li GL, Hou XL, Wan XR, Zhang ZB (2015) Sheep grazing causes shift in sex ratio and cohort structure of Brandt’s vole: implication of their adaptation to food shortage. Integr Zool. doi: 10.1111/1749-4877.12163 Google Scholar
  24. Lin LJ et al (2012) Growth of sheep as affected by grazing system and grazing intensity in the steppe of Inner Mongolia, China. Livest Sci 144:140–147. doi: 10.1016/j.livsci.2011.11.008 CrossRefGoogle Scholar
  25. Lindroth RL, Batzli GO (1984) Plant phenolics as chemical defenses: effects of natural phenolics on survival and growth of prairie voles (Microtus Ochrogaster). J Chem Ecol 10:229–244. doi: 10.1007/Bf00987851 PubMedCrossRefGoogle Scholar
  26. Lindroth RL, Batzli GO (1986) Inducible plant-chemical defenses: a cause of vole population cycles. J Anim Ecol 55:431–449. doi: 10.2307/4729 CrossRefGoogle Scholar
  27. Lindsey HA, Gallie J, Taylor S, Kerr B (2013) Evolutionary rescue from extinction is contingent on a lower rate of environmental change. Nature 494:463–467. doi: 10.1038/Nature11879 PubMedCrossRefGoogle Scholar
  28. Makkar HPS, Blummel M, Borowy NK, Becker K (1993) Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. J Sci Food Agr 61:161–165. doi: 10.1002/jsfa.2740610205 CrossRefGoogle Scholar
  29. Milchunas DG, Lauenroth WK, Burke IC (1998) Livestock grazing: animal and plant biodiversity of shortgrass steppe and the relationship to ecosystem function. Oikos 83:65–74. doi: 10.2307/3546547 CrossRefGoogle Scholar
  30. Otis DL, Burnham KP, White GC, Anderson DR (1978) Statistical inference from capture data on closed animal populations. Wildlife Monogr 62:7–135Google Scholar
  31. Ozgul A, Getz LL, Oli MK (2004) Demography of fluctuating populations: temporal and phase-related changes in vital rates of Microtus ochrogaster. J Anim Ecol 73:201–215. doi: 10.1111/j.0021-8790.2004.00797.x CrossRefGoogle Scholar
  32. Parsons EWR, Maron JL, Martin TE (2013) Elk herbivory alters small mammal assemblages in high-elevation drainages. J Anim Ecol 82:459–467. doi: 10.1111/1365-2656.12009 PubMedCrossRefGoogle Scholar
  33. Pielke RA et al (2011) Land use/land cover changes and climate: modeling analysis and observational evidence. Wires Clim Change 2:828–850. doi: 10.1002/Wcc.144 CrossRefGoogle Scholar
  34. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3. 1–117.
  35. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, URL
  36. Redfield JA, Taitt MJ, Krebs CJ (1978) Experimental alteration of sex ratios in populations of Microtus townsendii, a field vole. Can J Zool 56:17–27. doi: 10.1139/Z78-003 CrossRefGoogle Scholar
  37. Saetnan ER, Skarpe C, Batzli GO (2012) Do sheep affect vole populations in alpine meadows of central Norway? J Mammal 93:1283–1291. doi: 10.1644/11-Mamm-a-226.1 CrossRefGoogle Scholar
  38. Schonbach P et al (2011) Grassland responses to grazing: effects of grazing intensity and management system in an Inner Mongolian steppe ecosystem. Plant Soil 340:103–115. doi: 10.1007/s11104-010-0366-6 CrossRefGoogle Scholar
  39. Steen H, Mysterud A, Austrheim G (2005) Sheep grazing and rodent populations: evidence of negative interactions from a landscape scale experiment. Oecologia 143:357–364. doi: 10.1007/s00442-004-1792-z PubMedCrossRefGoogle Scholar
  40. Torre I, Diaz M, Martinez-Padilla J, Bonal R, Vinuela J, Fargallo JA (2007) Cattle grazing, raptor abundance and small mammal communities in Mediterranean grasslands. Basic Appl Ecol 8:565–575. doi: 10.1016/j.baae.2006.09.016 CrossRefGoogle Scholar
  41. Vandyne GM, Heady HF (1965) Botanical composition of sheep and cattle diets on a mature annual range. Hilgardia 36:465–492CrossRefGoogle Scholar
  42. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139CrossRefGoogle Scholar
  43. Xie XH, Wen YL, Niu HX, Shi DZ, Zhang ZB (2012) Re-feeding evokes reproductive overcompensation of food-restricted Brandt’s voles. Physiol Behav 105:653–660. doi: 10.1016/j.physbeh.2011.09.026 PubMedCrossRefGoogle Scholar
  44. Zhang YM, Zhang ZB, Liu JK (2003a) Burrowing rodents as ecosystem engineers: the ecology and management of plateau zokors Myospalax fontanierii in alpine meadow ecosystems on the Tibetan Plateau. Mammal Rev 33:284–294. doi: 10.1046/j.1365-2907.2003.00020.x CrossRefGoogle Scholar
  45. Zhang ZB, Pech R, Davis S, Shi DZ, Wan XR, Zhong WQ (2003b) Extrinsic and intrinsic factors determine the eruptive dynamics of Brandt’s voles Microtus brandti in Inner Mongolia, China. Oikos 100:299–310. doi: 10.1034/j.1600-0706.2003.11810.x CrossRefGoogle Scholar
  46. Zhang MW et al (2014) Small mammal community succession on the beach of Dongting Lake, China after the Three Gorges Project. Integr Zool 9:294–308. doi: 10.1111/1749-4877.12073 PubMedCrossRefGoogle Scholar
  47. Zhong WQ, Wang MJ, Wan XR (1999) Ecological management of Brandt’s vole (Microtus brandti) in Inner Mongolia, China. In: Singleton GRHL, Leirs H, Zhang Z (eds) Ecologically-based management of rodent pests. ACIAR, Canberra, pp 199–214Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Guoliang Li
    • 1
    • 2
  • Baofa Yin
    • 1
    • 3
  • Xinrong Wan
    • 1
  • Wanhong Wei
    • 3
  • Guiming Wang
    • 4
  • Charles J. Krebs
    • 5
  • Zhibin Zhang
    • 1
    Email author
  1. 1.State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of ZoologyChinese Academy of SciencesBeijingChina
  2. 2.College of Life ScienceUniversity of Chinese Academy of SciencesBeijingChina
  3. 3.College of Bioscience and BiotechnologyYangzhou UniversityYangzhouChina
  4. 4.Department of Wildlife, Fisheries and AquacultureMississippi State UniversityStarkvilleUSA
  5. 5.Department of ZoologyUniversity of British ColumbiaVancouverCanada

Personalised recommendations