Winter activity rhythms of a rodent pest species in agricultural habitats

Abstract

Predation risk is the main factor affecting movements of mammal prey species. Here we assessed the activity patterns of a nearly endemic fossorial rodent, the Savi’s pine vole Microtus savii, in two agroecosystems in central Italy. Direct captures were carried out in cold months (December–March) with live-traps; sex and age were recorded for each captured individual following standard methods. Savi’s pine voles were mostly active during daytime in both study sites, with no differences between sexes or age classes. Night-time movements were mainly registered during waning moon nights and were severely restricted in bright moonlight. The activity pattern of Savi’s pine voles seems to support the hypothesis of predation avoidance. The most common predators of these small rodents are mainly active during bright nights, when visibility is highest, forcing voles to be more active aboveground during daylight hours as well as in the darkest nights. Efficient monitoring and trapping programmes should therefore take place in daylight hours to increase capture success and to reduce stress levels of the captured animals.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Abramsky Z, Strauss E, Subach A, Riechman A, Kotler BP (1996) The effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbyi and G. pyramidum. Oecologia 105:313–319

    PubMed  CAS  Google Scholar 

  2. Agostinelli C, Lund U (2013) R package “circular”: circular statistics (version 0.4-7). http:// r-forge.r-project.org/projects/circular/. Accessed on 24th July 2017

  3. Amori G, Castiglia R (2018) Mammal endemism in Italy: a review. Biogeographia 33:19–31. https://doi.org/10.21426/B633035335

    Article  Google Scholar 

  4. Amori G, Contoli L, Nappi A (2008) Mammalia II: Erinaceomorpha, Soricomorpha, Lagomorpha, Rodentia. Edizioni Calderini de Il Sole 24 Ore, Milano

    Google Scholar 

  5. Avenant N (2011) The potential utility of rodents and other small mammals as indicators of ecosystem ‘integrity’ of South African grasslands. Wildl Res 38:626–639

    Google Scholar 

  6. Bertolino S, Colangelo P, Mori E, Capizzi D (2015a) Good for management, not for conservation: an overview of research, conservation and management of Italian small mammals. Hystrix 26:25–35

    Google Scholar 

  7. Bertolino S, Asteggiano L, Saladini MA, Giordani L, Vittone G, Alma A (2015b) Environmental factors and agronomic practices associated with Savi’s pine vole abundance in Italian apple orchards. J Pest Sci 88:135–142

    Google Scholar 

  8. Calhoun JB (1945) Diel activity of the rodents, Microtus ochrogaster and Sigmodon hispidus hispidus. Ecology 26:251–273

    Google Scholar 

  9. Caltran S (2002) I roditori dannosi alle colture erbacee ed arboree si combattono durante l’inverno. Vita di Campagna 10:29–32

    Google Scholar 

  10. Carnevali L, Lovari S, Monaco A, Mori E (2016) Nocturnal activity of a diurnal species, the northern chamois, in a predator-free Alpine area. Behav Proc 126:101–107

    Google Scholar 

  11. Cavallini P, Lovari S (1991) Environmental factors influencing the use of habitat in the red fox, Vulpes vulpes. J Zool (Lond) 223:323–339

    Google Scholar 

  12. Cavallini P, Lovari S (1994) Home range, habitat selection and activity of the red fox in a Mediterranean coastal ecotone. Acta Theriol 39:279–287

    Google Scholar 

  13. Clotfelter ED, Pedersen AB, Cranford JA, Ram N, Snajdr EA, Nolan V, Ketterson ED (2007) Acorn mast drives long-term dynamics of rodent and songbird populations. Oecologia 154:493–503

    PubMed  Google Scholar 

  14. Daan S, Slopsema S (1978) Short-term rhythms in foraging behaviour of the common vole, Microtus arvalis. J Comp Physiol 127:215–227

    Google Scholar 

  15. Decoursey PJ, Pius S, Sandlin C, Wethey D, Schull J (1998) Relationship of circadian temperature and activity rhythms in two rodent species. Physiol Behav 65:457–463

    PubMed  CAS  Google Scholar 

  16. Dell’Agnello F, Mazza V, Martini M, Bertolino S, Capizzi D, Riga F, Zaccaroni M (2018a) Trap type and positioning: how to trap Savi’s pine vole using the tunnel system. Mammalia 84:350–354

    Google Scholar 

  17. Dell’Agnello F, Barfknecht R, Bertolino S, Capizzi D, Martini M, Mazza V, Riga F, Zaccaroni M (2018b) Consistent demographic trends in Savi’s pine vole between two distant areas in Central Italy. Folia Zool 67:35–42

    Google Scholar 

  18. Erkinaro E (1961) The seasonal change of the activity of Microtus agrestis. Oikos 12:157–163

    Google Scholar 

  19. Fanini L, Longo S, Cervo R, Roversi PF, Mazza G (2014) Daily activity and non-random occurrence of captures in the Asian palm weevils. Ethol Ecol Evol 26:195–203

    Google Scholar 

  20. Grinder MI, Krausman PR (2001) Home range, habitat use, and nocturnal activity of coyotes in an urban environment. J Wildl Manag 4:887–898

    Google Scholar 

  21. Grodzinski W (1962) Influence of food upon the diurnal activity of small rodents. Symp Theriol Praha 1:134–140

    Google Scholar 

  22. Halle S, Lehmann U (1987) Circadian activity patterns, photoperiodic responses and population cycles in voles. Oecologia 71:568–572

    PubMed  CAS  Google Scholar 

  23. Holmes ND, Griffiths R, Pott M, Alifano A, Will D, Wegmann AS, Russell JC (2015) Factors associated with rodent eradication failure. Biol Conserv 185:8–16

    Google Scholar 

  24. Jaksić FM (1982) Inadequacy of activity time as a niche difference: the case of diurnal and nocturnal raptors. Oecologia 52:171–175

    PubMed  Google Scholar 

  25. Lehmann U (1976) Short-term and circadian rhythms in the behaviour of the vole, Microtus agrestis (L.). Oecologia 23:185–199

    PubMed  Google Scholar 

  26. Lioy S, Mori E, Wauters LA, Bertolino S (2016) Weight operated see-saw feeding hoppers are not selective for red squirrels when greys are present. Mammal Biol 81:365–371

    Google Scholar 

  27. Liro A (1974) Renewal of burrows by the common vole as the indicator of its numbers. Acta Theriol 19:259–272

    Google Scholar 

  28. Lisická L, Losík J, Zejda J, Heroldová M, Nesvadbová J, Tkadlec E (2007) Measurement error in a burrow index to monitor relative population size in the common vole. Folia Zool 56:169–176

    Google Scholar 

  29. Lourenço R, Penteriani V, del Mar DM, Marchi-Bartolozzi M, Rabaça JE (2011) Kill before being killed: an experimental approach supports the predator-removal hypothesis as a determinant of intraguild predation in top predators. Behav Ecol Socibiol 65:1709–1714

    Google Scholar 

  30. Marks CA, Bloomfield TE (2006) Home-range size and selection of natal den and diurnal shelter sites by urban red foxes (Vulpes vulpes) in Melbourne. Wildl Res 33:339–347

    Google Scholar 

  31. Miller RS, Elton C (1955) Activity rhythms in the wood mouse, Apodemus sylvaticus and the bank vole, Clethrionomys glareolus. Proc Zool Soc London 125:505–519

    Google Scholar 

  32. Molsher RL, Gifford EJ, McIlroy JC (2000) Temporal, spatial and individual variation in the diet of red foxes (Vulpes vulpes) in Central New South Wales. Wildl Res 27:593–601

    Google Scholar 

  33. Monterroso P, Alves PC, Ferreras P (2013) Catch me if you can: diel activity patterns of mammalian prey and predators. Ethol 119:1044–1056

    Google Scholar 

  34. Mori E, Nourisson DH, Lovari S, Romeo G, Sforzi A (2014a) Self-defence may not be enough: moonlight avoidance in a large, spiny rodent. J Zool (Lond) 294:31–40

    Google Scholar 

  35. Mori E, Menchetti M, Dartora F (2014b) Evidence of carrion consumption behaviour in the long-eared owl Asio otus (Linnaeus, 1758) (Aves: Strigiformes: Strigidae). Ital J Zool 81:471–475

    Google Scholar 

  36. Mori E, Menchetti M (2019) Living with roommates in a shared den: spatial and temporal segregation among semifossorial mammals. Behav Proc 164:48–53

    Google Scholar 

  37. Mukherjee S, Zelcer M, Kotler BP (2009) Patch use in time and space for a meso-predator in a risky world. Oecologia 159:661–668

    PubMed  Google Scholar 

  38. Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecol Monogr 57:111–128

    Google Scholar 

  39. Nichols JD (1992) Capture-recapture models. BioScience 42:94–102

    Google Scholar 

  40. Osella G, Montolli A (1986) La micromammalofauna di una stazione planiziaria piemontese. Hystrix 1:119–136

    Google Scholar 

  41. Patriarca E, Debernardi P (1997) Insectivora, Chiroptera, Lagomorpha, Rodentia and Carnivora of the Gran Paradiso National Park: checklist and preliminary ecological characterization Ibex. J Mount Ecol 4:17–32

    Google Scholar 

  42. Penteriani V, del Mar DM, Campioni L, Lourenço R (2010) Moonlight makes owls more chatty. PLoS One 5:e8696

    PubMed  PubMed Central  Google Scholar 

  43. Prugh LR, Golden CD (2014) Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles. J Anim Ecol 83:504–514

    PubMed  Google Scholar 

  44. Ranchelli E, Barfknecht R, Capizzi D, Riga F, Mazza V, Dell’Agnello F, Zaccaroni M (2016) From biology to management of Savi’s pine vole (Microtus savii). Pest Manag Sci 72:857–863

    PubMed  CAS  Google Scholar 

  45. Rowsemitt CN (1986) Seasonal variations in activity rhythms of male voles: mediation by gonadal hormones. Physiol Behav 37:797–803

    PubMed  CAS  Google Scholar 

  46. Salvioni M (1988a) Rhythmes d’activitè de trios espèces de Pitymys: Pitymys multiplex, P. savii and P. subterraneus (Mammalia, Rodentia). Mammalia 52:483–496

    Google Scholar 

  47. Salvioni M (1988b) Home range and social behaviour of three species of European Pitymys (Mammalia, Rodentia). Behav Ecol Sociobiol 22:203–210

    Google Scholar 

  48. Soe E, Davison J, Süld K, Saarma U (2017) Europe-wide biogeographical patternsin the diet of an ecologically and epidemiologically important mesopredator, the red fox Vulpes vulpes: a quantitative review. Mammal Rev 47:198–211

    Google Scholar 

  49. Somogyi BA, Horvàth GF (2018) Seasonal activity of common vole (Microtus arvalis) in alfalfa fields in southern Hungary. Biologia 74:9196. https://doi.org/10.2478/s11756-018-0149-8

    Article  Google Scholar 

  50. Speakman JR (1999) The cost of living: field metabolic rates of small mammals. Adv Ecol Res 30:177–297

    Google Scholar 

  51. Umhang G, Richomme C, Boucher JM, Guedon G, Boué F (2013) Nutrias and muskrats as bioindicators for the presence of Echinococcus multilocularis in new endemic areas. Vet Parasit 197:283–287

    Google Scholar 

Download references

Acknowledgements

We thank Raimund Grau, Ralf Barfknecht, Jörg Hahne and Emmanuelle Bonneris for their support.

Funding

The study was funded by Bayer CropScience.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marco Zaccaroni.

Ethics declarations

Animal trapping and handling procedures took place in compliance with the European Council Directives 92/43EEC and 86/609/EEC and the national regulations for animal research (D. Lgs 157/92 and D. Lgs 116/92).

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by: Joanna Stojak

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dell’Agnello, F., Martini, M., Mori, E. et al. Winter activity rhythms of a rodent pest species in agricultural habitats. Mamm Res 65, 69–74 (2020). https://doi.org/10.1007/s13364-019-00443-4

Download citation

Keywords

  • Agroecosystems
  • Microtus savii
  • Savi’s pine vole
  • Predation risk
  • Moonlight avoidance