Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Fertilisation, cattle grazing and voles: collapse of meadow vole populations in young forests?

Thomas P. Sullivan A C and Druscilla S. Sullivan B
+ Author Affiliations
- Author Affiliations

A Department of Forest and Conservation Sciences, Faculty of Forestry, University of British Columbia, 2424 Main Mall, Vancouver, British Columbia, V6T 1Z4, Canada.

B Applied Mammal Research Institute, 11010 Mitchell Avenue, Summerland, British Columbia, V0H 1Z8, Canada.

C Corresponding author. Email: tom.sullivan@ubc.ca

Wildlife Research 41(5) 367-378 https://doi.org/10.1071/WR13209
Submitted: 6 December 2013  Accepted: 1 October 2014   Published: 20 February 2015

Abstract

Context: A puzzling aspect of microtine population fluctuations is the damping out or collapsing of cycles over the last three decades, particularly in northern Europe. Occasional population fluctuations of Microtus may also have been damped out in temperate and boreal forests of the Pacific North-west of North America. One cause might be the presence of cattle (Bos taurus) grazing in forest habitats that offer summer forage.

Aims: We tested hypotheses (H) that abundance, population fluctuations, and demographic parameters of reproduction, recruitment and survival, of Microtus pennsylvanicus would be driven by understory plant productivity. Two predictions follow from this hypothesis: (H1) enhanced abundance and demography in fertilised stands, and (H2) reduced abundance and demography in stands with cattle grazing.

Methods: Study areas were located in ‘grazed’ and ‘ungrazed’ young forests in south-central British Columbia, Canada. Each study area had four replicate units of unfertilised and repeatedly fertilised stands. Herbaceous vegetation and meadow vole (M. pennsylvanicus) populations were sampled from 1993 to 2002.

Key results: Mean abundance of total herbs, grasses, and fireweed (Epilobium angustifolium) increased dramatically (8 to 34 times higher) with fertilisation in the ungrazed stands. Mean abundance of meadow voles was 3.1 to 8.5 times higher in the nutrient-enriched herbaceous vegetation in the ungrazed fertilised than grazed fertilised stands. Demographic variables also followed this pattern of abundance. Except for two years, mean abundance of meadow voles was similar between fertilised and unfertilised stands at the grazed area, with some degree of fluctuations generated in grazed stands. Thus, H1 and H2 were at least partly supported for M. pennsylvanicus in fertilised stands.

Conclusions: In high-quality habitats where cover and other attributes of vegetation are substantial enough to generate population increases and fluctuations of Microtus, grazing of vegetation by cattle or other livestock may indeed lead to potential collapse of fluctuations. Degree of grazing pressure would be crucial, but considering the widespread nature of grazing in the continuum of post-harvest forested sites in the Pacific North-west of North America, moderate to heavy grazing pressure is common.

Implications: Reductions in populations of microtines have serious consequences for predator communities and other ecological functions.

Additional keywords: cattle grazing, collapse of fluctuations, forest fertilisation, meadow voles, Microtus pennsylvanicus, population dynamics.


References

Adler, G. H. (1989). Demography of the meadow vole along a simple habitat gradient. Canadian Journal of Zoology 67, 772–774.
Demography of the meadow vole along a simple habitat gradient.Crossref | GoogleScholarGoogle Scholar |

Anderson, T. J., and Barrett, G. W. (1982). Effects of dried sewage sludge on meadow vole (Microtus pennsylvanicus) populations in two grassland communities. Journal of Applied Ecology 19, 759–772.
Effects of dried sewage sludge on meadow vole (Microtus pennsylvanicus) populations in two grassland communities.Crossref | GoogleScholarGoogle Scholar |

Batzli, G. O. (1985). Nutrition. In ‘Biology of New World Microtus’. (Ed. R. H. Tamarin.) pp. 779–811. (Special Publication Number 8. American Society of Mammalogists, Boston, MA.)

Batzli, G. O. (1992). Dynamics of small mammal populations: a review. In ‘Wildlife 2001: Populations’. (Eds D. R. McCullough and R. H. Barrett.) pp. 831–850. (Elsevier Applied Science: New York.)

Birney, E. C., Grant, W. E., and Baird, D. D. (1976). Importance of vegetative cover to cycles of Microtus populations. Ecology 57, 1043–1051.
Importance of vegetative cover to cycles of Microtus populations.Crossref | GoogleScholarGoogle Scholar |

Boonstra, R., Krebs, C. J., Gilbert, S., and Schweiger, S. (2001). Voles and mice. In ‘Ecosystem Dynamics of the Boreal Forest’. (Eds C. J. Krebs, S. Boutin and R. Boonstra.) pp. 215–239. (Oxford University Press: Oxford.)

Boutin, S. (1990). Food supplementation experiments with terrestrial vertebrates: patterns, problems and the future. Canadian Journal of Zoology 68, 203–220.
Food supplementation experiments with terrestrial vertebrates: patterns, problems and the future.Crossref | GoogleScholarGoogle Scholar |

Brockley, R. P. (2005). Effects of post-thinning density and repeated fertilization on the growth and development of young lodgepole pine. Canadian Journal of Forest Research 35, 1952–1964.
Effects of post-thinning density and repeated fertilization on the growth and development of young lodgepole pine.Crossref | GoogleScholarGoogle Scholar |

Brommer, J. E., Pietiainen, H., Ahola, K., Karell, P., Karstinen, T., and Kolunen, H. (2010). The return of the vole cycle in southern Finland refutes the generality of the loss of cycles through “climate forcing”. Global Change Biology 16, 577–586.
The return of the vole cycle in southern Finland refutes the generality of the loss of cycles through “climate forcing”.Crossref | GoogleScholarGoogle Scholar |

Chapman, E. W., and Ribic, C. A. (2002). The impact of buffer strips and stream-side grazing on small mammals in southwestern Wisconsin. Agriculture, Ecosystems & Environment 88, 49–59.
The impact of buffer strips and stream-side grazing on small mammals in southwestern Wisconsin.Crossref | GoogleScholarGoogle Scholar |

Christensen, P., and Hörnfeldt, B. (2003). Long-term decline of vole populations in northern Sweden: a test of the destructive sampling hypothesis. Journal of Mammalogy 84, 1292–1299.
Long-term decline of vole populations in northern Sweden: a test of the destructive sampling hypothesis.Crossref | GoogleScholarGoogle Scholar |

Cornulier, T., Yoccoz, N. G., Bretagnolle, V., Brommer, J. E., Butet, A., Ecke, F., Elston, D. A., Framstad, E., Henttonen, H., Hörnfeldt, B., Huitu, O., Imholt, C., Ims, R. A., Jacob, J., Jędrzejewska, B., Millon, A., Petty, S. J., Pietiäinen, H., Tkadlec, E., Zub, K., and Lambin, X. (2013). Europe-wide dampening of population cycles in keystone herbivores. Science 340, 63–66.
Europe-wide dampening of population cycles in keystone herbivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVCrsr4%3D&md5=26f8814272b5e846ec3d0be3d566ef46CAS | 23559246PubMed |

Craig, V. J., Klenner, W., Feller, M. C., and Sullivan, T. P. (2014). Population dynamics of meadow voles (Microtus pennsylvanicus) and long-tailed voles (M. longicaudus) and their relationship to downed wood in managed forests. Mammal Research , .
Population dynamics of meadow voles (Microtus pennsylvanicus) and long-tailed voles (M. longicaudus) and their relationship to downed wood in managed forests.Crossref | GoogleScholarGoogle Scholar |

Evans, D. M., Redpath, S. M., Elston, D. A., Evans, S. A., Mitchell, R. J., and Dennis, P. (2006). To graze or not to graze? Sheep, voles, forestry and nature conservation in the British uplands. Journal of Applied Ecology 43, 499–505.
To graze or not to graze? Sheep, voles, forestry and nature conservation in the British uplands.Crossref | GoogleScholarGoogle Scholar |

Fisher, J. T., and Wilkinson, L. (2005). The response of mammals to forest fire and timber harvest in the North American boreal forest. Mammal Review 35, 51–81.
The response of mammals to forest fire and timber harvest in the North American boreal forest.Crossref | GoogleScholarGoogle Scholar |

Fowler, J., Cohen, L., and Jarvis, P. (1998). ‘Practical Statistics for Field Biology.’ 2nd edn. (John Wiley and Sons: Chichester, UK.)

Getz, L. L. (1985). Habitats. In ‘Biology of New World Microtus’. (Ed. R. H. Tamarin.) pp. 286–309. (Special Publication Number 8. American Society of Mammalogists, Boston, MA.)

Grant, W. E., French, N. R., and Swift, D. M. (1977). Response of a small mammal community to water and nitrogen treatments in a shortgrass prairie ecosystem. Journal of Mammalogy 58, 637–652.
Response of a small mammal community to water and nitrogen treatments in a shortgrass prairie ecosystem.Crossref | GoogleScholarGoogle Scholar |

Hall, A. T., Woods, P. E., and Barrett, G. W. (1991). Population dynamics of the meadow vole (Microtus pennsylvanicus) in nutrient-enriched old-field communities. Journal of Mammalogy 72, 332–342.
Population dynamics of the meadow vole (Microtus pennsylvanicus) in nutrient-enriched old-field communities.Crossref | GoogleScholarGoogle Scholar |

Hansson, L. (1989). Landscape and habitat dependence in cyclic and semi-cyclic small rodents. Holarctic Ecology 12, 345–350.

Hipkiss, T., Stefansson, O., and Hörnfeldt, B. (2008). Effect of cyclic and declining food supply on great grey owls in boreal Sweden. Canadian Journal of Zoology 86, 1426–1431.
Effect of cyclic and declining food supply on great grey owls in boreal Sweden.Crossref | GoogleScholarGoogle Scholar |

Hitchcock, C. L., and Cronquist, A. (1973). ‘Flora of the Pacific Northwest.’ (University of Washington Press: Seattle, WA.)

Hörnfeldt, B. (2004). Long-term decline in numbers of cyclic voles in boreal Sweden: analysis and presentation of hypotheses. Oikos 107, 376–392.
Long-term decline in numbers of cyclic voles in boreal Sweden: analysis and presentation of hypotheses.Crossref | GoogleScholarGoogle Scholar |

Hörnfeldt, B., Christensen, P., Sandstrom, P., and Ecke, F. (2006). Long-term decline and local extinction of Clethrionomys rufocanus in boreal Sweden. Landscape Ecology 21, 1135–1150.
Long-term decline and local extinction of Clethrionomys rufocanus in boreal Sweden.Crossref | GoogleScholarGoogle Scholar |

Huntly, N., and Inouye, R. S. (1987). Small mammal populations of an old-field chronosequence: successional patterns and associations with vegetation. Journal of Mammalogy 68, 739–745.
Small mammal populations of an old-field chronosequence: successional patterns and associations with vegetation.Crossref | GoogleScholarGoogle Scholar |

Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54, 187–211.
Pseudoreplication and the design of ecological field experiments.Crossref | GoogleScholarGoogle Scholar |

Huynh, H., and Feldt, L. S. (1976). Estimation of the Box correction for degrees of freedom from sample data in the randomized block and split-plot designs. Journal of Statistics Education 1, 69–82.
Estimation of the Box correction for degrees of freedom from sample data in the randomized block and split-plot designs.Crossref | GoogleScholarGoogle Scholar |

Ims, R. A., Henden, J.-A., and Killengreen, S. T. (2008). Collapsing population cycles. Trends in Ecology & Evolution 23, 79–86.
Collapsing population cycles.Crossref | GoogleScholarGoogle Scholar |

Jędrzejewski, W., and Jedrzejewska, B. (1996). Productivity of ground vegetation and predation in the Palearctic. Acta Theriologica 41, 1–34.
Productivity of ground vegetation and predation in the Palearctic.Crossref | GoogleScholarGoogle Scholar |

Johnston, A. N., and Anthony, R. G. (2008). Small-mammal microhabitat associations and response to grazing in Oregon. The Journal of Wildlife Management 72, 1736–1746.
Small-mammal microhabitat associations and response to grazing in Oregon.Crossref | GoogleScholarGoogle Scholar |

Jolly, G. M., and Dickson, J. M. (1983). The problem of unequal catachability in mark-recapture estimation of small mammal populations. Canadian Journal of Zoology 61, 922–927.
The problem of unequal catachability in mark-recapture estimation of small mammal populations.Crossref | GoogleScholarGoogle Scholar |

Kellner, O., and Redbo-Torstensson, P. (1995). Effects of elevated nitrogen deposition on the field-layer vegetation in coniferous forests. Ecological Bulletins 44, 227–237.

Körpimäki, E., and Krebs, C. J. (1996). Predation and population cycles of small mammals. Bioscience 46, 754–764.
Predation and population cycles of small mammals.Crossref | GoogleScholarGoogle Scholar |

Krebs, C. J. (1996). Population cycles revisited. Journal of Mammalogy 77, 8–24.
Population cycles revisited.Crossref | GoogleScholarGoogle Scholar |

Krebs, C. J. (1999). ‘Ecological Methodology.’ (Addison Wesley Longman: Menlo Park, CA.)

Krebs, C. J. (2013). ‘Population Fluctuations in Rodents.’ (The University of Chicago Press: Chicago, IL.)

Krebs, C. J., and Boonstra, R. (1984). Trappability estimates for mark-recapture data. Canadian Journal of Zoology 62, 2440–2444.
Trappability estimates for mark-recapture data.Crossref | GoogleScholarGoogle Scholar |

Krebs, C. J., Keller, B. L., and Tamarin, R. H. (1969). Microtus population biology: demographic changes in fluctuating populations of M. ochrogaster and M. pennsylvanicus in southern Indiana. Ecology 50, 587–607.
Microtus population biology: demographic changes in fluctuating populations of M. ochrogaster and M. pennsylvanicus in southern Indiana.Crossref | GoogleScholarGoogle Scholar |

Krebs, C. J., Boonstra, R., Gilbert, S., Reid, D., Kenney, A. J., and Hofer, E. J. (2011). Density estimation for small mammals from livetrapping grids: rodents in northern Canada. Journal of Mammalogy 92, 974–981.
Density estimation for small mammals from livetrapping grids: rodents in northern Canada.Crossref | GoogleScholarGoogle Scholar |

Kuehl, R. O. (1994). Repeated measures designs. In ‘Statistical Principles of Research Design and Analysis’. pp. 499–528. (Duxbury Press: Belmont, CA.)

Laine, K., and Henttonen, H. (1983). The role of plant production in microtine cycles in northern Fennoscandia. Oikos 40, 407–418.
The role of plant production in microtine cycles in northern Fennoscandia.Crossref | GoogleScholarGoogle Scholar |

Lindgren, P. M. F., Sullivan, T. P., Sullivan, D. S., Brockley, R. P., and Winter, R. (2007). Growth response of young lodgepole pine to thinning and repeated fertilization treatments: 10-year results. Forestry 80, 587–611.
Growth response of young lodgepole pine to thinning and repeated fertilization treatments: 10-year results.Crossref | GoogleScholarGoogle Scholar |

Littel, R. C. (1989). Statistical analysis of experiments with repeated measures. HortScience 24, 36–40.

Meidinger, D., and Pojar, J. (1991). Ecosystems of British Columbia. Research Branch Ministry of Forests, Victoria, B.C. Special Report Series No. 6.

Oksanen, T., Schneider, M., Rammul, U., Hamback, P., and Aunapuu, M. (1999). Population fluctuations of voles in northern Fennoscandian tundra: contrasting dynamics in adjacent areas with different habitat composition. Oikos 86, 463–478.
Population fluctuations of voles in northern Fennoscandian tundra: contrasting dynamics in adjacent areas with different habitat composition.Crossref | GoogleScholarGoogle Scholar |

Peles, J. D., and Barrett, G. W. (1996). Effects of vegetative cover on the population dynamics of meadow voles. Journal of Mammalogy 77, 857–869.
Effects of vegetative cover on the population dynamics of meadow voles.Crossref | GoogleScholarGoogle Scholar |

Quinton, D. A. (1984). Cattle diets on seeded clearcut areas in central interior British Columbia. Journal of Range Management 37, 349–352.
Cattle diets on seeded clearcut areas in central interior British Columbia.Crossref | GoogleScholarGoogle Scholar |

Saetnan, E. R., Skarpe, C., and Batzli, G. O. (2012). Do sheep affect vole populations in alpine meadows of central Norway? Journal of Mammalogy 93, 1283–1291.
Do sheep affect vole populations in alpine meadows of central Norway?Crossref | GoogleScholarGoogle Scholar |

Seber, G. A. F. (1982). ‘The Estimation of Animal Abundance and Related Parameters.’ 2nd edn. (Charles Griffin: London.)

SPSS Institute Inc (2007). Statistical Programs for the Social Sciences. SPSS Institute Inc., Chicago, IL.

Stenseth, N. C. (1999). Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos 87, 427–461.
Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world.Crossref | GoogleScholarGoogle Scholar |

Stickney, P. F. (1985). Data base for early post-fire succession on the sundance burn, northern Idaho. USDA Forest Service, Intermountain Research Station. General Technical Report INT-189.

Sullivan, T. P., and Sullivan, D. S. (2001). Influence of variable retention harvests on forest ecosystems. II. Diversity and population dynamics of small mammals. Journal of Applied Ecology 38, 1234–1252.
Influence of variable retention harvests on forest ecosystems. II. Diversity and population dynamics of small mammals.Crossref | GoogleScholarGoogle Scholar |

Sullivan, T. P., and Sullivan, D. S. (2010). Forecasting vole population outbreaks in forest plantations: the rise and fall of a major mammalian pest. Forest Ecology and Management 260, 983–993.
Forecasting vole population outbreaks in forest plantations: the rise and fall of a major mammalian pest.Crossref | GoogleScholarGoogle Scholar |

Sullivan, T. P., Sullivan, D. S., Lindgren, P. M. F., and Ransome, D. B. (2006). Influence of repeated fertilization on forest ecosystems: relative abundance and habitat use by snowshoe hares. Canadian Journal of Forest Research 36, 2080–2089.
Influence of repeated fertilization on forest ecosystems: relative abundance and habitat use by snowshoe hares.Crossref | GoogleScholarGoogle Scholar |

Sullivan, T. P., Sullivan, D. S., and Lindgren, P. M. F. (2008). Influence of variable retention harvests on forest ecosystems: plant and mammal responses up to 8 years post-harvest. Forest Ecology and Management 254, 239–254.
Influence of variable retention harvests on forest ecosystems: plant and mammal responses up to 8 years post-harvest.Crossref | GoogleScholarGoogle Scholar |

Sullivan, T. P., Sullivan, D. S., and Lindgren, P. M. F. (2012). Influence of repeated fertilization and cattle grazing on forest ecosystems: abundance and diversity of forest-floor small mammals. Forest Ecology and Management 277, 180–195.
Influence of repeated fertilization and cattle grazing on forest ecosystems: abundance and diversity of forest-floor small mammals.Crossref | GoogleScholarGoogle Scholar |

Sundell, J., Huitu, O., Henttonen, H., Kaikusalo, A., Korpimaki, E., Pietiainen, H., Saurola, P., and Hanski, I. (2004). Large-scale spatial dynamics of vole populations in Finland revealed by the breeding success of vole-eating avian predators. Journal of Animal Ecology 73, 167–178.
Large-scale spatial dynamics of vole populations in Finland revealed by the breeding success of vole-eating avian predators.Crossref | GoogleScholarGoogle Scholar |

Taitt, M. J., and Krebs, C. J. (1985). Population dynamics and cycles. In ‘Biology of New World Microtus’. (Ed. R. H. Tamarin.) pp. 567–620. (Special Publication Number 8. American Society of Mammalogists, Boston, MA.)

Turkington, R., John, E., and Dale, M. R. T. (2001). Plant dynamics: herbs and grasses. In ‘Ecosystem Dynamics of the Boreal Forest’. (Eds C. J. Krebs, S. Boutin, and R. Boonstra.) pp. 70–91. (Oxford University Press: Oxford, UK.)

Van Horne, B. (1982). Demography of the long-tail vole Microtus longicaudus in seral stages of coastal coniferous forest, southeast Alaska. Canadian Journal of Zoology 60, 1690–1709.
Demography of the long-tail vole Microtus longicaudus in seral stages of coastal coniferous forest, southeast Alaska.Crossref | GoogleScholarGoogle Scholar |

VanderSchaaf, C. L., Moore, J. A., and Kingery, J. L. (2000). The effect of multi-nutrient fertilization on understory plant diversity. Northwest Science 74, 316–324.

Villar, N., Lambin, X., Evans, D., Pakeman, R., and Redpath, S. (2013). Experimental evidence that livestock grazing intensity affects the activity of a generalist predator. Acta Oecologica 49, 12–16.
Experimental evidence that livestock grazing intensity affects the activity of a generalist predator.Crossref | GoogleScholarGoogle Scholar |

Villar, N., Cornulier, T., Evans, D., Pakeman, R., Redpath, S., and Lambin, X. (2014). Experimental evidence that livestock grazing intensity affects cyclic vole population regulation processes. Population Ecology 56, 55–61.
Experimental evidence that livestock grazing intensity affects cyclic vole population regulation processes.Crossref | GoogleScholarGoogle Scholar |

Wikeem, B. M., McLean, A., Bawtree, A., and Quinton, D. (1993). An overview of the forage resource and beef production on Crown land in British Columbia. Canadian Journal of Animal Science 73, 779–794.
An overview of the forage resource and beef production on Crown land in British Columbia.Crossref | GoogleScholarGoogle Scholar |

Willms, W., McLean, A., Tucker, R., and Ritcey, R. (1980). Deer and cattle diets on summer range in British Columbia. Journal of Range Management 33, 55–59.
Deer and cattle diets on summer range in British Columbia.Crossref | GoogleScholarGoogle Scholar |

Wilson, K. R., and Anderson, D. R. (1985). Evaluation of two density estimators of small mammal population size. Journal of Mammalogy 66, 13–21.
Evaluation of two density estimators of small mammal population size.Crossref | GoogleScholarGoogle Scholar |

Zar, J. H. (1999). ‘Biostatistical Analysis,’ 4th edn. (Prentice-Hall, Inc.: Englewood Cliffs, NJ.)