Road effects on demographic traits of small mammal populations

  • Ana Galantinho
  • Sofia Eufrázio
  • Carmo Silva
  • Filipe Carvalho
  • Russell Alpizar-Jara
  • António Mira
Original Article

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.

Keywords

Apodemus sylvaticus Capture-recapture Extended robust design models Population estimation Roadless area Road effects 

Supplementary material

10344_2017_1076_MOESM1_ESM.pdf (66 kb)
ESM 1(PDF 66 kb)

References

  1. 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, 141–149Google Scholar
  2. 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 21:3681–3697CrossRefGoogle Scholar
  3. 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:e0151500CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s Information Criterion. J Wildl Manag 74:1175–1178CrossRefGoogle Scholar
  5. Barrows CW, Allen MF, Rotenberry JT (2006) Boundary processes between a desert sand dune community and an encroaching suburban landscape. Biol Conserv 131:486–494CrossRefGoogle Scholar
  6. Bailey LL, Simons TR, Pollock KH (2004) Estimating detection probability parameters for Plethodon salamanders using the robust capture–recapture design. J Wildl Manag 68:1–13CrossRefGoogle Scholar
  7. Bellamy PE, Shore RF, Ardeshir D, Treweek JR, Sparks TH (2000) Road verges as habitat for small mammals in Britain. Mammal Rev 30:131–139CrossRefGoogle Scholar
  8. 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 143:1307–1316CrossRefGoogle Scholar
  9. Bennett AF (1990) Habitat corridors and the conservation of small mammals in a fragmented forest environment. Landsc Ecol 4:109–122CrossRefGoogle Scholar
  10. 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 253:513–521CrossRefGoogle Scholar
  11. Bissonette JA, Rosa SA (2009) Road zone effects in small-mammal communities. Ecol Soc 14:27CrossRefGoogle Scholar
  12. Borges FJA, Marini MA (2010) Birds nesting survival in disturbed and protected neotropical savannas. Biodivers Conserv 19:223–236CrossRefGoogle Scholar
  13. Borchers DL, Buckland ST, Zucchini W (2002) Estimating animal abundance: closed populations. Springer-Verlag, LondonCrossRefGoogle Scholar
  14. Brandstätter E (1999) Confidence intervals as an alternative to significance testing. Method Psych Res Online 4:33–46Google Scholar
  15. Brock RE, Kelt DA (2004) Influence of roads on the endangered Stephens kangaroo rat (Dipodomys stephensi): are dirt and gravel roads different? Biol Conserv 118:633–640CrossRefGoogle Scholar
  16. 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, MarylandGoogle Scholar
  17. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information—theoretic approach, 2nd edn. Springer-Verlag, New YorkGoogle Scholar
  18. 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 57:157–174CrossRefGoogle Scholar
  19. CGE (2011) Dados Meteorológicos do Centro de Geofísica de Évora. CGE, Universidade de Évora, Évora. http:// www.cge.uevora.pt/. Accessed 25 May 2011
  20. Cooch EG, White GC (2013) Program MARK: a gentle introduction. http://www.phidot.org/software/mark/docs/book. Accessed 26 Jun 2013
  21. 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 53:181–190CrossRefGoogle Scholar
  22. 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 144:1335–1346CrossRefGoogle Scholar
  23. Díaz M, Alonso CL (2003) Wood mouse Apodemus sylvaticus winter food supply: density, condition, breeding, and parasites. Ecol 84:2680–2691CrossRefGoogle Scholar
  24. Downing RJ, Rytwinski T, Fahrig L (2015) Positive effects of roads on small mammals: a test of the predation release hypothesis. Ecol Res 30:651–662CrossRefGoogle Scholar
  25. Efford M (1992) Comment—revised estimates of the bias in ‘minimum number alive’ estimator. Can J Zool 70:628–631CrossRefGoogle Scholar
  26. EP (2005) Recenseamento do tráfego – Évora. Estradas de Portugal, E.P.E.Google Scholar
  27. Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol Soc 14:21CrossRefGoogle Scholar
  28. Ford AT, Fahrig L (2008) Movement patterns of eastern chipmunks (Tamias striatus) near roads. J Mammal 89:895–903CrossRefGoogle Scholar
  29. 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, DCGoogle Scholar
  30. 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 49:113–122CrossRefGoogle Scholar
  31. Getz LL, Cole FR, Gates DL (1978) Interstate roadsides as dispersal routes for Microtus pennsylvanicus. J Mammal 59:208–212CrossRefGoogle Scholar
  32. Goosem M (2000) Effects of tropical rainforest roads on small mammals: edge changes in community composition. Wildl Res 27:151–163CrossRefGoogle Scholar
  33. Gurnell J (1978) Seasonal changes in numbers and male behavioural interaction in a population of wood mice, Apodemus sylvaticus. J Anim Ecol 47:741–755CrossRefGoogle Scholar
  34. Gurnell J, Flowerdew JR (2006) Live trapping small mammals. A practical guide. The Mammal Society, LondonGoogle Scholar
  35. 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 404–407Google Scholar
  36. Kendall WL, Pollock KH, Brownie C (1995) A likelihood-based approach to capture-recapture estimation of demographic parameters under the robust design. Biometrics 51:293-308Google Scholar
  37. Kendall WL, Nichols JD, Hines JE (1997) Estimating temporary emigration using capture-recapture data with Pollock’s robust design. Ecol 78:563–578Google Scholar
  38. 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 180:53–61CrossRefGoogle Scholar
  39. Legendre P (2011) lmodel2: Model II Regression. R package version 1.7–0. http://CRAN.R-project.org/package=lmodel2
  40. Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549CrossRefPubMedGoogle Scholar
  41. Macpherson D, Macpherson JL, Morris P (2011) Rural roads as barriers to the movements of small mammals. Appl Ecol Environ Res 9:167–180CrossRefGoogle Scholar
  42. Mañosa S, Cordero PJ (1992) Seasonal and sexual variation in the diet of the common buzzard in Northeastern Spain. J Raptor Res 26:235–238Google Scholar
  43. Marcheselli M, Sala L, Mauri M (2010) Bioaccumulation of PGEs and other traffic-related metals in populations of the small mammal Apodemus sylvaticus. Chemosphere 80:1247–1254CrossRefPubMedGoogle Scholar
  44. McGregor RL, Bender DJ, Fahrig L (2008) Do small mammals avoid roads because of the traffic? J Appl Ecol 45:117–123CrossRefGoogle Scholar
  45. Meunier F, Gauriat C, Verheyden C, Jouventin P (1999) Bird communities of highway verges: influence of adjacent habitat and roadside management. Acta Oecol 20:1–13CrossRefGoogle Scholar
  46. Montgomery WI (1989a) Population regulation in the wood mouse, Apodemus sylvaticus. I. Density dependence in the annual cycle of abundance. J Anim Ecol 58:465–475CrossRefGoogle Scholar
  47. Montgomery WI (1989b) Population regulation in the wood mouse, Apodemus sylvaticus. II. Density dependence in spatial distribution and reproduction. J Anim Ecol 58:477–494CrossRefGoogle Scholar
  48. Musser G, Ruedas L (2008) Niviventer cameroni. The IUCN Red List of Threatened Species 2008:e.T136512A4302696Google Scholar
  49. 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:e91942CrossRefGoogle Scholar
  50. Oxley DJ, Fenton MB, Carmody GR (1974) The effects of roads on populations of small mammals. J Appl Ecol 11:51–59CrossRefGoogle Scholar
  51. Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332CrossRefGoogle Scholar
  52. 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 62:369–373CrossRefGoogle Scholar
  53. 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
  54. Pinto-Correia T, Mascarenhas J (1999) Contribution to the extensification/intensification debate: new trends in the Portuguese montado. Landsc Urban Plan 46:125–131CrossRefGoogle Scholar
  55. Pita R, Mira A, Beja P (2006) Conserving the Cabrera vole, Microtus cabrerae, in intensively used Mediterranean landscapes. Agric Ecosyst Environ 115:1–5CrossRefGoogle Scholar
  56. Planillo A, Malo JE (2013) Motorway verges: paradise for prey species? A case study with the European rabbit. Mamm Biol 78:187–192Google Scholar
  57. Pollock KH (1982) A capture-recapture design robust to unequal probability of capture. J Wildl Manag 46:752–757CrossRefGoogle Scholar
  58. Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture–recapture experiments. Wildl Monogr 107:1–97Google Scholar
  59. 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 13:105–119CrossRefGoogle Scholar
  60. 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/
  61. Redon L, Machon N, Kerbiriou C, Jiguet F (2010) Possible effects of roadside verges on vole outbreaks in an intensive agrarian landscape. Mamm Biol 75:92–94Google Scholar
  62. Rosário IT, Mathias ML (2004) Annual weight variation and reproductive cycle of the wood mouse (Apodemus sylvaticus) in a Mediterranean environment. Mamm 68:133–140CrossRefGoogle Scholar
  63. Ruiz-Capillas P, Mata C, Malo JE (2013) Road verges are refuges for small mammal populations in extensively managed Mediterranean landscapes. Biol Conserv 158:223–229CrossRefGoogle Scholar
  64. 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 30:417–427CrossRefGoogle Scholar
  65. 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 26:277–287CrossRefGoogle Scholar
  66. Sanders TA, Trost RE (2013) Use of capture–recapture models with mark-resight data to estimate abundance of Aleutian cackling geese. J Wildl Manag 77:1459–1471CrossRefGoogle Scholar
  67. Sarmento P (1996) Feeding ecology of the European wildcat Felis silvestris in Portugal. Acta Theriol 41:409–414CrossRefGoogle Scholar
  68. 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 38:233–244CrossRefGoogle Scholar
  69. 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 92:235–253CrossRefGoogle Scholar
  70. 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 144:1742–1752CrossRefGoogle Scholar
  71. Sokal RR, Rohlf JR (1997) Biometry: the principles and practice of statistic in biological research, 3rd edn. WH Freeman and Company, New YorkGoogle Scholar
  72. 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:e66399CrossRefPubMedPubMedCentralGoogle Scholar
  73. Torres A, Jaeger JAG, Alonso JC (2016) Assessing large-scale wildlife responses to human infrastructure development. Proc Nat Acad Sci 113:8472–8477CrossRefPubMedPubMedCentralGoogle Scholar
  74. van Horne B (1983) Density as a misleading indicator of habitat quality. J Wildl Manag 47:893–901CrossRefGoogle Scholar
  75. Wang G, Getz LL (2007) State-space models for stochastic and seasonal fluctuations of vole and shrew populations in east-central Illinois. Ecol Model 207:189–196CrossRefGoogle Scholar
  76. Ware HE, McClure CJW, Carlisle JD, Barber JR (2015) A phantom road experiment reveals traffic noise is an invisible source of habitat degradation. PNAS 112:12105–12109CrossRefPubMedPubMedCentralGoogle Scholar
  77. 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 MexicoGoogle Scholar
  78. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139CrossRefGoogle Scholar
  79. 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 53:83–98Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.UBC - Unidade de Biologia da Conservação, Departamento de BiologiaUniversidade de ÉvoraÉvoraPortugal
  2. 2.CIBIO-UE - Centro de Investigação em Biodiversidade e Recursos Genéticos, Pólo de Évora, Grupo de Investigação em Ecologia AplicadaUniversidade de ÉvoraÉvoraPortugal
  3. 3.ICAAM - Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Grupo de Investigação em Paisagem, Biodiversidade e Sistemas Sócio-EcológicosUniversidade de ÉvoraÉvoraPortugal
  4. 4.Department of Zoology and Entomology, School of Biological and Environmental SciencesUniversity of Fort HareAliceSouth Africa
  5. 5.Centro de Investigação em Matemática e Aplicações, Instituto de Investigação e Formação Avançada, Departamento de Matemática, Escola de Ciências e TecnologiaUniversidade de ÉvoraÉvoraPortugal

Personalised recommendations