Skip to main content
Log in

Road effects on demographic traits of small mammal populations

  • Original Article
  • Published:
European Journal of Wildlife Research Aims and scope Submit manuscript

Abstract

Recent studies have highlighted the positive effects of road verges on the abundance of small mammals. However, most of these studies occurred in intensively grazed or cultivated areas, where verges were the last remnants of suitable habitats, which could mask the true effects of roads on population traits. We analysed the effects of roads on small mammal populations living in a well-preserved Mediterranean forest. We used the wood mouse (Apodemus sylvaticus) as a model of forest-dwelling small mammals that probably are among the species most affected by road clearings. Our study compared populations in similar habitat areas with and without road influence. We assessed abundance, survival and temporary emigration using extended Pollock’s robust design capture-recapture models. Moreover, we analysed population turnover, sex ratio, age structure and body condition. We found that wood mouse abundance and body condition were lower at the road bisected area, whereas the remaining population traits were similar. This suggests that the reduced habitat availability and quality due to the physical presence of the road and verge vegetation clearing are the main drivers of demographic differences in wood mouse populations between areas. Nevertheless, our results also suggest that in high-quality habitats surrounding national roads, wood mouse populations present similar dynamics to others living in undisturbed areas, despite the decrease in abundance and body condition. Overall, the often-reported increased small mammal abundance in road surroundings should not be generalized independently of habitat quality or to other population traits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alcántara M, Díaz M (1996) Patterns of body weight, body size, and body condition in the wood mouse Apodemus sylvaticus l.: effects of sex and habitat quality. Proc I Eur Congr Mammal, Museu Bocage, Lisboa, 141–149

  • Ascensão F, Clevenger AP, Grilo C, Filipe J, Santos-Reis M (2012) Highway verges as habitat providers for small mammals in agrosilvopastoral environments. Biodivers Conserv 21:3681–3697

    Article  Google Scholar 

  • Ascensão F, Mata C, Malo JE, Ruiz-Capillas P, Silva C, Silva AP, Santos-Reis M, Fernandes C (2016) Disentangle the causes of the road barrier effect in small mammals through genetic patterns. PLoS One 11:e0151500

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s Information Criterion. J Wildl Manag 74:1175–1178

    Article  Google Scholar 

  • Barrows CW, Allen MF, Rotenberry JT (2006) Boundary processes between a desert sand dune community and an encroaching suburban landscape. Biol Conserv 131:486–494

    Article  Google Scholar 

  • Bailey LL, Simons TR, Pollock KH (2004) Estimating detection probability parameters for Plethodon salamanders using the robust capture–recapture design. J Wildl Manag 68:1–13

    Article  Google Scholar 

  • Bellamy PE, Shore RF, Ardeshir D, Treweek JR, Sparks TH (2000) Road verges as habitat for small mammals in Britain. Mammal Rev 30:131–139

    Article  Google Scholar 

  • Benítez-López A, Alkemade R, Verweij PA (2010) The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biol Conserv 143:1307–1316

    Article  Google Scholar 

  • Bennett AF (1990) Habitat corridors and the conservation of small mammals in a fragmented forest environment. Landsc Ecol 4:109–122

    Article  Google Scholar 

  • Bertolino S, Viano C, Currado I (2001) Population dynamics, breeding patterns and spatial use of the garden dormouse (Eliomys quercinus) in an Alpine habitat. J Zool 253:513–521

    Article  Google Scholar 

  • Bissonette JA, Rosa SA (2009) Road zone effects in small-mammal communities. Ecol Soc 14:27

    Article  Google Scholar 

  • Borges FJA, Marini MA (2010) Birds nesting survival in disturbed and protected neotropical savannas. Biodivers Conserv 19:223–236

    Article  Google Scholar 

  • Borchers DL, Buckland ST, Zucchini W (2002) Estimating animal abundance: closed populations. Springer-Verlag, London

    Book  Google Scholar 

  • Brandstätter E (1999) Confidence intervals as an alternative to significance testing. Method Psych Res Online 4:33–46

    Google Scholar 

  • Brock RE, Kelt DA (2004) Influence of roads on the endangered Stephens kangaroo rat (Dipodomys stephensi): are dirt and gravel roads different? Biol Conserv 118:633–640

    Article  Google Scholar 

  • Burnham KP, Anderson DR, White GC, Brownie C, Pollock KH (1987) Design and analysis methods for fish survival experiments based on release-recapture. American Fisheries Society Monograph 5, Bethesda, Maryland

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information—theoretic approach, 2nd edn. Springer-Verlag, New York

    Google Scholar 

  • Carvalho F, Mira A (2011) Comparing annual vertebrate road kills over two time periods, 9 years apart: a case study in Mediterranean farmland. Eur J Wildl Res 57:157–174

    Article  Google Scholar 

  • CGE (2011) Dados Meteorológicos do Centro de Geofísica de Évora. CGE, Universidade de Évora, Évora. http:// www.cge.uevora.pt/. Accessed 25 May 2011

  • Cooch EG, White GC (2013) Program MARK: a gentle introduction. http://www.phidot.org/software/mark/docs/book. Accessed 26 Jun 2013

  • D’Amico M, Périquet S, Román J, Revilla E (2016) Road avoidance responses determine the impact of heterogeneous road networks at a regional scale. J App Ecol 53:181–190

    Article  Google Scholar 

  • Delibes-Mateos M, Smith AT, Slobodchikoff CN, Swenson JE (2011) The paradox of keystone species persecuted as pests: a call for the conservation of abundant small mammals in their native range. Biol Conserv 144:1335–1346

    Article  Google Scholar 

  • Díaz M, Alonso CL (2003) Wood mouse Apodemus sylvaticus winter food supply: density, condition, breeding, and parasites. Ecol 84:2680–2691

    Article  Google Scholar 

  • Downing RJ, Rytwinski T, Fahrig L (2015) Positive effects of roads on small mammals: a test of the predation release hypothesis. Ecol Res 30:651–662

    Article  Google Scholar 

  • Efford M (1992) Comment—revised estimates of the bias in ‘minimum number alive’ estimator. Can J Zool 70:628–631

    Article  Google Scholar 

  • EP (2005) Recenseamento do tráfego – Évora. Estradas de Portugal, E.P.E.

  • Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol Soc 14:21

    Article  Google Scholar 

  • Ford AT, Fahrig L (2008) Movement patterns of eastern chipmunks (Tamias striatus) near roads. J Mammal 89:895–903

    Article  Google Scholar 

  • Forman RTT, Sperling D, Bissonette JA, Clevenger AP, Cutshall CD, Dale VH, Fahrig L, France R, Goldman CR, Heanue K, Jones JA, Swanson FJ, Turrentine T, Winter TC (2003) Road ecology. Island Press, Washington, DC

    Google Scholar 

  • Garratt CG, Minderman J, Whittingham MJ (2012) Should we stay or should we go now? What happens to small mammals when grass is mown, and the implications for birds of prey. Ann Zool Fennici 49:113–122

    Article  Google Scholar 

  • Getz LL, Cole FR, Gates DL (1978) Interstate roadsides as dispersal routes for Microtus pennsylvanicus. J Mammal 59:208–212

    Article  Google Scholar 

  • Goosem M (2000) Effects of tropical rainforest roads on small mammals: edge changes in community composition. Wildl Res 27:151–163

    Article  Google Scholar 

  • Gurnell J (1978) Seasonal changes in numbers and male behavioural interaction in a population of wood mice, Apodemus sylvaticus. J Anim Ecol 47:741–755

    Article  Google Scholar 

  • Gurnell J, Flowerdew JR (2006) Live trapping small mammals. A practical guide. The Mammal Society, London

    Google Scholar 

  • Jubete F (2002) Apodemus sylvaticus (Linnaeus, 1785). In: Palomo LJ, Gisbert J (eds) Atlas de los Mamíferos terrestres de España. Dirección General de Conservación de la Naturaleza-SECEM-SECEM, Madrid, pp 404–407

    Google Scholar 

  • Kendall WL, Pollock KH, Brownie C (1995) A likelihood-based approach to capture-recapture estimation of demographic parameters under the robust design. Biometrics 51:293-308

  • Kendall WL, Nichols JD, Hines JE (1997) Estimating temporary emigration using capture-recapture data with Pollock’s robust design. Ecol 78:563–578

    Google Scholar 

  • La Haye MJJ, Swinnen KRR, Kuiters AT, Leirs H, Siepel H (2014) Modelling population dynamics of the common hamster (Cricetus cricetus): timing of harvest as a critical aspect in the conservation of a highly endangered rodent. Biol Conserv 180:53–61

    Article  Google Scholar 

  • Legendre P (2011) lmodel2: Model II Regression. R package version 1.7–0. http://CRAN.R-project.org/package=lmodel2

  • Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549

    Article  PubMed  Google Scholar 

  • Macpherson D, Macpherson JL, Morris P (2011) Rural roads as barriers to the movements of small mammals. Appl Ecol Environ Res 9:167–180

    Article  Google Scholar 

  • Mañosa S, Cordero PJ (1992) Seasonal and sexual variation in the diet of the common buzzard in Northeastern Spain. J Raptor Res 26:235–238

    Google Scholar 

  • Marcheselli M, Sala L, Mauri M (2010) Bioaccumulation of PGEs and other traffic-related metals in populations of the small mammal Apodemus sylvaticus. Chemosphere 80:1247–1254

    Article  CAS  PubMed  Google Scholar 

  • McGregor RL, Bender DJ, Fahrig L (2008) Do small mammals avoid roads because of the traffic? J Appl Ecol 45:117–123

    Article  Google Scholar 

  • Meunier F, Gauriat C, Verheyden C, Jouventin P (1999) Bird communities of highway verges: influence of adjacent habitat and roadside management. Acta Oecol 20:1–13

    Article  Google Scholar 

  • Montgomery WI (1989a) Population regulation in the wood mouse, Apodemus sylvaticus. I. Density dependence in the annual cycle of abundance. J Anim Ecol 58:465–475

    Article  Google Scholar 

  • Montgomery WI (1989b) Population regulation in the wood mouse, Apodemus sylvaticus. II. Density dependence in spatial distribution and reproduction. J Anim Ecol 58:477–494

    Article  Google Scholar 

  • Musser G, Ruedas L (2008) Niviventer cameroni. The IUCN Red List of Threatened Species 2008:e.T136512A4302696

    Google Scholar 

  • Navarro-Castillla A, Mata C, Ruiz-Capillas P, Palme R, Malo JE, Barja I (2014) Are motorways potential stressors of roadside wood mice (Apodemus sylvaticus) populations? PLoS One 9:e91942

    Article  Google Scholar 

  • Oxley DJ, Fenton MB, Carmody GR (1974) The effects of roads on populations of small mammals. J Appl Ecol 11:51–59

    Article  Google Scholar 

  • Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332

    Article  Google Scholar 

  • Pezzo F, Morimando F (1995) Food habits of the barn owl, Tyto alba, in a Mediterranean rural area: comparison with the diet of two sympatric carnivores. Bol Zool 62:369–373

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015). nlme: linear and nonlinear mixed effects models. R package version 3.1–120. http://cran.r-project.org/package=nlme

  • Pinto-Correia T, Mascarenhas J (1999) Contribution to the extensification/intensification debate: new trends in the Portuguese montado. Landsc Urban Plan 46:125–131

    Article  Google Scholar 

  • Pita R, Mira A, Beja P (2006) Conserving the Cabrera vole, Microtus cabrerae, in intensively used Mediterranean landscapes. Agric Ecosyst Environ 115:1–5

    Article  Google Scholar 

  • Planillo A, Malo JE (2013) Motorway verges: paradise for prey species? A case study with the European rabbit. Mamm Biol 78:187–192

    Google Scholar 

  • Pollock KH (1982) A capture-recapture design robust to unequal probability of capture. J Wildl Manag 46:752–757

    Article  Google Scholar 

  • Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture–recapture experiments. Wildl Monogr 107:1–97

    Google Scholar 

  • Pollock KH, Nichols JD, Simons TR, Farnsworth GL, Bailey LL, Sauer JR (2002) Large scale wildlife monitoring studies: statistical methods for design and analysis. Environmetrics 13:105–119

    Article  Google Scholar 

  • R Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07-0, http://www.R-project.org/

  • Redon L, Machon N, Kerbiriou C, Jiguet F (2010) Possible effects of roadside verges on vole outbreaks in an intensive agrarian landscape. Mamm Biol 75:92–94

    Google Scholar 

  • Rosário IT, Mathias ML (2004) Annual weight variation and reproductive cycle of the wood mouse (Apodemus sylvaticus) in a Mediterranean environment. Mamm 68:133–140

    Article  Google Scholar 

  • Ruiz-Capillas P, Mata C, Malo JE (2013) Road verges are refuges for small mammal populations in extensively managed Mediterranean landscapes. Biol Conserv 158:223–229

    Article  Google Scholar 

  • Ruiz-Capillas P, Mata C, Malo JE (2015) How many rodents die on the road? Biological and methodological implications from a small mammals’ roadkill assessment on a Spanish motorway. Ecol Res 30:417–427

    Article  Google Scholar 

  • Sabino-Marques H, Mira A (2011) Living on the verge: are roads a more suitable refuge for small mammals than streams in Mediterranean pastureland? Ecol Res 26:277–287

    Article  Google Scholar 

  • Sanders TA, Trost RE (2013) Use of capture–recapture models with mark-resight data to estimate abundance of Aleutian cackling geese. J Wildl Manag 77:1459–1471

    Article  Google Scholar 

  • Sarmento P (1996) Feeding ecology of the European wildcat Felis silvestris in Portugal. Acta Theriol 41:409–414

    Article  Google Scholar 

  • Serafini P, Lovari S (1993) Food habits and trophic niche overlap of the red fox and the stone marten in a Mediterranean rural area. Acta Theriol 38:233–244

    Article  Google Scholar 

  • Sikes RS, Gannon WL, Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253

    Article  Google Scholar 

  • Silva S, Ranjeewa ADG, Weerakoon D (2011) Demography of Asian elephants (Elephas maximus) at Uda Walawe National Park, Sri Lanka based on identified individuals. Biol Conserv 144:1742–1752

    Article  Google Scholar 

  • Sokal RR, Rohlf JR (1997) Biometry: the principles and practice of statistic in biological research, 3rd edn. WH Freeman and Company, New York

    Google Scholar 

  • Tête N, Fritsch C, Afonso E, Coeurdassier M, Lambert J-C, Giraudoux P, Scheifler R (2013) Can body condition and somatic indices be used to evaluate metal-induced stress in wild small mammals? PLoS One 8:e66399

    Article  PubMed  PubMed Central  Google Scholar 

  • Torres A, Jaeger JAG, Alonso JC (2016) Assessing large-scale wildlife responses to human infrastructure development. Proc Nat Acad Sci 113:8472–8477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Horne B (1983) Density as a misleading indicator of habitat quality. J Wildl Manag 47:893–901

    Article  Google Scholar 

  • Wang G, Getz LL (2007) State-space models for stochastic and seasonal fluctuations of vole and shrew populations in east-central Illinois. Ecol Model 207:189–196

    Article  Google Scholar 

  • Ware HE, McClure CJW, Carlisle JD, Barber JR (2015) A phantom road experiment reveals traffic noise is an invisible source of habitat degradation. PNAS 112:12105–12109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White GC, Anderson DR, Burnham KP, Otis DL (1982) Capture-recapture and removal methods for sampling closed populations. Los Alamos National Laboratory, Los Alamos, New Mexico

    Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139

    Article  Google Scholar 

  • Zuberogoitia I, Martínez JE, Martínez JA, Zabala J, Calvo JF, Castillo I, Azkona A, Iraeta A, Hidalgo S (2006) Influence of management practices on nest site habitat selection, breeding and diet of the common buzzard Buteo buteo in two different areas of Spain. Ardeola 53:83–98

    Google Scholar 

Download references

Acknowledgements

This study was funded by the Portuguese Foundation for Science and Technology (FCT; POPH/FSE) through a PhD grant attributed to AG (SFRH/BD/66382/2009). Unidade de Biologia da Conservação (UBC) and Instituto de Ciências Agrárias e Ambientais Mediterrânicas (ICAAM) provided additional funding. We thank the landowners for allowing us to use their land. We are grateful to André Lourenço, André Silva, Clara Ferreira, Denis Medinas, Edgar Gomes, Helena Marques, Marta Duarte, Pedro Costa, Rafael Carvalho, Sara Valente and Tiago Marques for the kind assistance in different stages of data collection. We thank the valuable comments from Ricardo Pita and Sara Santos. We thank the suggestions from the handling editor and two anonymous reviewers that greatly improved our paper. We also thank the support from the analysis forum at http://www.phidot.org.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Galantinho.

Ethics declarations

This research involves animals.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All the procedures followed the guidelines approved by the Portuguese Institute for Nature and Forest Conservation (ICNF - Instituto de Conservação da Natureza e das Florestas) and the American Society of Mammalogists for the use of wild mammals in research (Sikes et al. 2011).

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 66 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Galantinho, A., Eufrázio, S., Silva, C. et al. Road effects on demographic traits of small mammal populations. Eur J Wildl Res 63, 22 (2017). https://doi.org/10.1007/s10344-017-1076-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10344-017-1076-7

Keywords

Navigation