Mammalian Biology

, Volume 81, Issue 4, pp 372–379 | Cite as

Wood mouse population dynamics: Interplay among seed abundance seasonality, shrub cover and wild boar interference

  • Pau SunyerEmail author
  • Alberto Muñoz
  • Marc J. Mazerolle
  • Raúl Bonal
  • Josep Maria Espelta
Original investigation


Small rodents play a key role in forest ecosystems as common prey, but also as prevalent seed consumers and dispersers. Hence, there is a great interest in disentangling the factors involved in their population dynamics. We conducted an intensive 2-year field study to test the relative role of seasonality in seed abundance, shrub cover and wild boar interference on the population dynamics of wood mice, Apodemus sylvaticus, in a Mediterranean oak forest. Wood mice demographic parameters varied strongly with the seasonal variations in acorn availability on the ground. Mice survival and abundance dropped drastically during summer, the period of acorn scarcity, but rose again in autumn when acorn-fall began. Specifically, female abundance was associated with the temporal changes in acorn availability on the ground, but were randomly distributed in space whereas males showed a spatially aggregated pattern during the acorn-abundant seasons (autumn-winter). In contrast to studies conducted in sparse oak forests in drier environments, spatial variability in shrub cover and wild boar foraging activity did not affect directly the population dynamics of wood mice. This could be due to the presence of an abundant shrub layer and a closed canopy in our forest that enhance environmental conditions and provides shelter against predators and ungulates. Our study highlights that the relative importance of environmental factors and intraguild competition on rodent dynamics may be highly context-dependent, varying greatly among different sites. We suggest that the relationships between acorn dispersers and oaks are more reciprocal than previously considered.


Apodemus sylvaticus Demographic parameters Mediterranean Quercus ilex Quercus pubescens Rodents Sus scrofa 


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  1. Bates, D., Maechler, M., Bolker, B., 2011. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42.
  2. Blondel, J., Aronson, J., 1999. Biology and Wildlife of Mediterranean Region. Oxford University Press, Oxford.Google Scholar
  3. Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd ed. Springer-Verlag, New York.Google Scholar
  4. Burnham, K.P., Anderson, D.R., White, G.C., Brownie, C, Pollock, K.H., 1987. Design and analysis methods for fish survival experiments based on release-recapture. Am. Fish. Soc. Monogr., 5.Google Scholar
  5. Cahill, S., Llimona, F., Gràcia, J., 2003. Spacing and nocturnal activity of wild boar Sus scrofa in a Mediterranean metropolitan park, Wildl. Biol. 9, 3–13.CrossRefGoogle Scholar
  6. Cheveau, M., Drapeau, P., Imbeau, L, Bergeron, Y., 2004. Owl winter irruptions as an indicator of small mammal population cycles in the boreal forest of eastern North America, Oikos 107, 190–198.CrossRefGoogle Scholar
  7. Choquet, R., Lebreton, J.D., Gimenez, O., Reboulet, A.M., Pradel, R., 2009. U-CARE: utilities for performing goodness of fit tests and manipulating CApture-REcapture data, Ecography 32, 1071–1074.CrossRefGoogle Scholar
  8. Den Ouden, J., Jansen, P.A., Smit, R., 2005. Jays, mice and oaks: Predation and dispersal of Quercus robur and Q. petraea in North-western Europe. In: Forget, P.M., Lambert, J., Vander Wall, S.B. (Eds.), Seed Fate: Predation, Dispersal and Seedling Establishment. CABI Publising, Wallingford, pp. 223–240.CrossRefGoogle Scholar
  9. Daniel, J.A., Potter, K., Altom, W., Aljoe, H., Stevens, R., 2002. Long-term grazing density impacts on soil compaction, Trans. ASAE 45, 1911–1915.CrossRefGoogle Scholar
  10. Díaz, M., Torre, I., Arrizabalaga, A., 2010. Relative roles of density and rainfall on the short-term regulation of Mediterranean wood mouse Apodemus sylvaticus populations, Acta Theriol. 55, 251–260.CrossRefGoogle Scholar
  11. Espelta, J.M., Cortés, P., Molowny-Horas, R., Sánchez-Humanes, B., Retana, J., 2008. Masting mediated by summer drought reduces acorn predation in Mediterranean oak forests, Ecology 89, 805–817.PubMedCrossRefPubMedCentralGoogle Scholar
  12. Espelta, J.M., Bonal, R., Sánchez-Humanes, B., 2009a. Pre-dispersal acorn predation in mixed oak forests: interspecific differences are driven by the interplay among seed phenology, seed size and predator size. J. Ecol. 97, 1416–1423.CrossRefGoogle Scholar
  13. Espelta, J.M., Cortés, P., Molowny-Horas, R., Retana, J., 2009b. Acorn crop and pre-dispersal predation determine inter-specific differences in the recruitment of co-occurring oaks. Oecologia 161, 559–568.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Fernandez, F.A.S., Evans, P.R., Dunstone, N., 1996. Population dynamics of the wood mouse Apodemus sylvaticus (Rodentia: Muridae) in a Sitka spruce successional mosaic, J. Zool. 239, 717–730.CrossRefGoogle Scholar
  15. Focardi, S., Capizzi, D., Monetti, D., 2000. Competition for acorns among wild boar (Sus scrofa) and small mammals in a Mediterranean woodland, J. Zool. 250, 329–334.CrossRefGoogle Scholar
  16. Fons, R., Saint-Girons, M.C., 1993. Le cycle sexuel chez le mulot sylvestre Apodemus sylvaticus (L., 1758) en région méditerranéenne, Mamm. Biol. 58, 38–47.Google Scholar
  17. Godsall, B., Coulson, T., Malo, A., 2014. From physiology to space use: energy reserves and androgenization explain home-range size variation in a woodland rodent, J. Anim. Ecol. 83, 126–135.PubMedCrossRefGoogle Scholar
  18. Gómez, J.M., Hódar, J.A., 2008. Wild boars (Sus scrofa) affect the recruitment rate and spatial distribution of Holm oak (Quercus ilex), For. Ecol. Manag. 256, 1384–1389.CrossRefGoogle Scholar
  19. Gómez, J.M., Puerta-Piñero, C, Schupp, E.W., 2008. Effectiveness of rodents as local seed dispersers of Holm oaks, Oecologia 155, 529–537.PubMedCrossRefGoogle Scholar
  20. Herrera, C, 1995. Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants, Annu. Rev. Ecol. Syst. 26, 705–727.CrossRefGoogle Scholar
  21. Hollander, J.L., Vander Wall, S.B., 2004. Effectiveness of six species of rodents as dispersers of singleleaf piñon pine (Pinus monophylla), Oecologia 138, 57–65.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Huggins, R.M., 1989. On the statistical analysis of capture-recapture experiments, Biometrika 76, 133–140.CrossRefGoogle Scholar
  23. Khammes, N., Aulagnier, S., 2007. Diet of the wood mouse, Apodemus sylvaticus in three biotopes of Kabylie of Djurdjura (Algeria), Folia Zool. 56 (3), 243–252.Google Scholar
  24. Kotler, B.P., Brown, J.S., Slotow, R.H., Goodfriend, W.L., Strauss, M., 1993. The influence of snakes on the foraging behavior of gerbils. Oikos 53, 145–152.CrossRefGoogle Scholar
  25. Laake, J., Rakimberdiev, E., Collier, B., Rotella, J., Paul, A., 2012. RMark: R Code for MARK Analysis. R package version 2.1.0.
  26. Mazerolle, M.J., 2006. Improving data analysis in herpetology: using Akaike’s information criterion (AIC) to assess the strength of biological hypotheses, Amphibia-Reptilia 27, 169–180.CrossRefGoogle Scholar
  27. Mazerolle, M.J., 2015. AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 2.0.-3.
  28. Montgomery, W.I., 1989a. Population regulation in the wood mouse, Apodemus sylvaticus: I. Density dependence in the annual cycle of abundance. J. Anim. Ecol. 58, 465–475.Google Scholar
  29. Montgomery, W.I., 1989b. Population regulation in the wood mouse: Apodemus sylvaticus. II. Density dependence in spatial distribution and reproduction. J. Anim. Ecol. 58, 477–494.Google Scholar
  30. Montgomery, W.I., Wilson, W.L., Hamilton, R., McCartney, P., 1991. Dispersion in the wood mouse, Apodemus sylvaticus: variable resources in time and space, J. Anim. Ecol. 60, 179–192.CrossRefGoogle Scholar
  31. Montgomery, W.I., 1999. Apodemus sylvaticus (Linnaeus, 1758). In: Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Krystufek, B., Reijnders, P.J.H., Spitzenberger, F., Stubbe, M., Thissen, J.B.M., Vohralík, V., Zima, J. (Eds.), The Atlas of European Mammals. T and AD Poyser, Carlton, pp. 274–275.Google Scholar
  32. Mun˜oz, A., Bonal, R., 2007. Rodents change acorn dispersal behaviour in response to ungulate presence, Oikos 116, 1631–1638.CrossRefGoogle Scholar
  33. Mun˜oz, A., Bonal, R., 2008. Seed choice by rodents: learning or inheritance? Behav, Ecol. Sociobiol. 62, 913–922.CrossRefGoogle Scholar
  34. Mun˜oz, A., Bonal, R., Díaz, M., 2009. Ungulates rodents, shrubs: interactions in a diverse Mediterranean ecosystem, Basic Appl. Ecol. 10, 151–160.CrossRefGoogle Scholar
  35. Perea, R., San Miguel, A., Gil, L., 2011a. Acorn dispersal by rodents: the importance of re-dispersal and distance to shelter. Basic Appl. Ecol. 12, 432–439.CrossRefGoogle Scholar
  36. Perea, R., González, R., San Miguel, A., Gil, L., 2011b. Moonlight and shelter cause differential seed selection and removal by rodents. Anim. Behav. 82, 717–723.CrossRefGoogle Scholar
  37. Perry, J.N., Hewitt, M., 1991. A new index of aggregation for animal counts, Biometrics 47, 1505–1518.PubMedCrossRefGoogle Scholar
  38. Perry, J.N., Winder, L., Holland, J.M., Alston, R.D., 1999. Red-blue plots for detecting clusters in count data, Ecol. Lett. 2, 106–113.CrossRefGoogle Scholar
  39. Pollock, K.H., 1982. A capture-recapture design robust to unequal probability of capture, J. Wildl. Manag. 46, 752–757.CrossRefGoogle Scholar
  40. Pons, J., Pausas, J.G., 2012. The coexistence of acorns with different maturation patterns explains acorn production variability in Cork oak, Oecologia 169, 723–731.PubMedCrossRefGoogle Scholar
  41. Pulido, F., Díaz, M., 2005. Regeneration of a Mediterranean oak: a whole-cycle approach, Écoscience 12, 92–102.CrossRefGoogle Scholar
  42. Rajska-Jurgiel, E., 1992. Demography of woodland rodents in fragmented habitat. Acta Theriol. 37 (1-2), 73–90.CrossRefGoogle Scholar
  43. R Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL Scholar
  44. Rosalino, L.M., Ferreira, D., Leitão, I., Santos-Reis, M., 2011. Selection of nest sites by wood mice Apodemus sylvaticus in a Mediterranean agro-forest landscape, Ecol. Res. 26, 445–452.CrossRefGoogle Scholar
  45. Rosário, I.T., Mathias, M.L., 2004. Annual weight variation and reproductive cycle of the wood mouse (Apodemus sylvaticus) in a Mediterranean environment. Mammalia 68 (2-3), 133–140.CrossRefGoogle Scholar
  46. Saitoh, T., Vik, J.O., Stenseth, N.C., Takanishi, T., Hayakashi, S., Ishida, N., Ohmori, M., Morita, T., Uemura, S., Kadomatsu, M., Osawa, J., Maekawa, K., 2008. Effects of acorn abundance on density dependence in a Japanese wood mouse (Apodemus speciosus) population, Popul. Ecol. 50, 159–167.CrossRefGoogle Scholar
  47. Schradin, C, 2005. Nest-site competition in two diurnal rodents from the succulent karoo of South Africa, J. Mammal. 86, 757–762.CrossRefGoogle Scholar
  48. Shimada, T., Saitoh, T., 2006. Re-evaluation ofthe relationship between rodent populations and acorn masting: a review from the aspect of nutrients and defensive chemicals in acorns, Popul. Ecol. 48, 341–352.CrossRefGoogle Scholar
  49. Smit, R., Bokdam, J., den Ouden, J., Olff, H., Schot-Opschoor, H., Schrijvers, M., 2001. Effects of introduction and exclusion of large herbivores on small rodent communities, Plant Ecol. 155, 119–127.CrossRefGoogle Scholar
  50. Sunyer, P., Muñoz, A., Bonal, R., Espelta, J.M., 2013. The ecology of seed dispersal by small rodents: a role for predator and conspecific scents, Funct. Ecol. 27, 1313–1321.CrossRefGoogle Scholar
  51. Sunyer, P., Espelta, J.M., Bonal, R., Muñoz, A., 2014. Seeding phenology influences wood mouse seed choices: the overlooked role of timing in the foraging decisions by seed-dispersing rodents, Behav. Ecol. Sociobiol. 68, 1205–1213.CrossRefGoogle Scholar
  52. Sunyer, P., Boixadera, E., Muñoz, A., Bonal, R., Espelta, J.M., 2015. The interplay among acorn abundance and rodent behavior drives the spatial pattern of seedling recruitment in mature Mediterranean oak forests. PLoS One 10 (6), e0129844.CrossRefGoogle Scholar
  53. Torre, I., Arrizabalaga, A., Díaz, M., 2002. Ratón de campo (Apodemus sylvaticus Linnaeus, 1758), Galemys 14, 1–26.Google Scholar
  54. Unnsteinsdottir, E.R., Hersteinsson, P., 2011. Effects of contrasting habitats on population parameters and diet of Apodemus sylvaticus (Rodentia) in south-western Iceland, Mammalia 75, 13–21.CrossRefGoogle Scholar
  55. Vander Wall, S.B., 2001. The evolutionary ecology of nut dispersal, Bot. Rev. 67, 74–117.CrossRefGoogle Scholar
  56. Vander Wall, S.B., 2010. How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals, Philos. Trans. R. Soc. B 365, 989–997.CrossRefGoogle Scholar
  57. White, G.C., Burnham, K.P., 1999. Program MARK: survival estimation from populations of marked animals, Bird Study 46, 120–138.CrossRefGoogle Scholar
  58. Zhang, H., Cheng, J., Xiao, Z., Zhang, Z., 2008. Effects of seed abundance on seed scatter-hoarding of Edward’s rat (Leopoldamys edwardsi Muridae) at the individual level, Oecologia 158, 57–63.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2016

Authors and Affiliations

  • Pau Sunyer
    • 1
    Email author
  • Alberto Muñoz
    • 1
    • 2
  • Marc J. Mazerolle
    • 3
    • 6
  • Raúl Bonal
    • 1
    • 4
    • 5
  • Josep Maria Espelta
    • 1
  1. 1.CREAFCataloniaSpain
  2. 2.Departamento de Didáctica de las Ciencias ExperimentalesFacultad de Educación, Universidad Complutense de MadridMadridSpain
  3. 3.Centre d’Étude de la ForêtUniversité du Québec en Abitibi-TémiscamingueQuébecCanada
  4. 4.Forest Research Group (GIF) INDEHESAUniversity of ExtremaduraPlasenciaSpain
  5. 5.DITEG Research GroupUniversity of Castilla-La ManchaToledoSpain
  6. 6.Centre d’étude de la forêt, Département des sciences du boiset de la forêtUniversité LavalQuébecCanada

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