Skip to main content

Advertisement

Log in

Humans do matter: determinants of red fox (Vulpes vulpes) presence in a western Mediterranean landscape

  • Original Paper
  • Published:
Mammal Research Aims and scope Submit manuscript

Abstract

Habitat loss, due to landscape changes induced by human activities, is considered one of the main drivers of biodiversity decline. Thus, understanding how these changes affect top trophic-level species is essential to develop effective conservation strategy measures to overcome this problem. Mesocarnivores, as higher trophic-level species with crucial roles in ecosystem functioning, are a pivotal functional group in such strategies. Generalist mesocarnivores, such as the red fox (Vulpes vulpes), are excellent models to study species ecological adaption to landscapes moulded by humans. Using generalised linear mixed model (GLMM), we aim to understand how the landscape context affects the presence of this generalist species, in a Mediterranean ecosystem (northeastern Portugal) characterised by a combination of natural areas and traditional agricultural land uses. Based on scats’ distribution, we generated distribution models to test different ecological hypotheses—anthropic disturbance factors, altitude and land-cover patterns. According to our results, red foxes seem to have two distinct strategies: in forest-dominated areas, human activities have a negative effect (disturbance); in areas with a low percentage of forests, agriculture patches and the proximity to urban areas are the main drivers determining its presence, with a positive influence (food availability). Our results confirm the opportunistic character of this species and its high degree of adaptation. Further, the outcome also reveals that landscape context influences the detected pattern. Consequently, considering that populations of the same species are constrained by the same factors, independently of the landscape composition, will affect the effectiveness of management measures that will not account for landscape context effects.

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

Data availability

The datasets generated during and/or analysed during the current study are not publicly available due to the fact that these are part of a major project that is under a confidentiality agreement until the project is finished but are available from the corresponding author on reasonable request. After the end of the project, data will be included and available at the ‘Atlas of Portuguese mammals’ website database: http://atlas-mamiferos.uevora.pt/index.php/downloads/.

References

  • Álvares F, Ferreira CC, Barbosa AM, Rosalino LM, Pedroso NM, Bencatel J (2017) Carnívoros. In: Bencatel J, Álvares F, Moura AE, Barbosa AM (eds) Atlas de Mamíferos de Portugal. Universidade de Évora, Portugal, pp 61–95

    Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s Information Criterion. J Wildl Manag 74:1175–1178. https://doi.org/10.2193/2009-367

    Article  Google Scholar 

  • Azevedo JC (2012) Florestas, ambiente e sustentabilidade: uma abordagem centrada nos serviços de ecossistemas das florestas do distrito de Bragança. Academia das Ciências de Lisboa, Lisboa

  • Baker PJ, Funk SM, Harris S, White PCL (2000) Flexible spatial organization of urban foxes, Vulpes vulpes, before and during an outbreak of sarcoptic mange. Anim Behav 59:127–146. https://doi.org/10.1006/ANBE.1999.1285

    Article  CAS  PubMed  Google Scholar 

  • Barea-Azcón JM, Virgós E, Ballesteros-Duperón E, Moleón M, Chirosa M (2007) Surveying carnivores at large spatial scales: a comparison of four broad-applied methods. Biodivers Conserv 16:1213–1230. https://doi.org/10.1007/s10531-006-9114

    Article  Google Scholar 

  • Barton, K., 2016. MuMIn: multi-model inference [WWW document]. R Packag. version 1.15.6. URL: https://cran.r-project.org/package=MuMIn (Accessed 28 June 2017)

  • Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287:1–23. https://doi.org/10.1111/j.1469-7998.2011.00887

    Article  Google Scholar 

  • Bencatel J, Ferreira CC, Barbosa AM, Rosalino LM, Álvares F (2018) Research trends and geographical distribution of mammalian carnivores in Portugal (SW Europe). PLoS One 13(11):e0207866. https://doi.org/10.1371/journal.pone.0207866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blalock HM (1963) Correlated independent variables: the problem of multicollinearity. Social Forces 42(2):233–237. https://doi.org/10.1093/sf/42.2.233

    Article  Google Scholar 

  • Blondel J (2006) The “design” of Mediterranean landscapes: a millennial story of humans and ecological systems during the historic period. Hum Ecol 34:713–729. https://doi.org/10.1007/s10745-006-9030-4

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York, NY

    Google Scholar 

  • Cabral MJ, Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira ME, Palmeirim JM, Queiroz AI, Rogado L, Santos-Reis M (2005) Livro vermelho dos vertebrados de Portugal. Instituto da Conservação da Natureza, Lisboa

    Google Scholar 

  • Carl G, Kühn I (2007) Analyzing spatial autocorrelation in species distributions using Gaussian and logit models. Ecol Model 207:159–170. https://doi.org/10.1016/J.ECOLMODEL.2007.04.024

    Article  Google Scholar 

  • Caro T (2010) Conservation by proxy: indicator, umbrella, keystone, flagship, and other surrogate species. Island Press, Washington

    Google Scholar 

  • Carvalho J, Torres RT, Acevedo P, Santos JPV, Barros T, Serrano E, Fonseca C (2017) Propagule pressure and land cover changes as main drivers of red and roe deer expansion in mainland Portugal. Divers Distrib 24:551–564. https://doi.org/10.1111/ddi.12703

    Article  Google Scholar 

  • Cavallini P (1996) Ranging behaviour of red foxes during the mating and breeding seasons. Ethol Ecol Evol 8(1):57–65. https://doi.org/10.1080/08927014.1996.9522935

    Article  Google Scholar 

  • Contesse P, Hegglin D, Gloor S, Bontadina F, Deplazes P (2004) The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zurich, Switzerland. Mamm Biol - Zeitschrift für Säugetierkd 69:81–95. https://doi.org/10.1078/1616-5047-00123

    Article  Google Scholar 

  • Cruz J, Sarmento P, White PCL (2015) Influence of exotic forest plantations on occupancy and co-occurrence patterns in a Mediterranean carnivore guild. J Mammal 96:854–865

    Article  Google Scholar 

  • Curveira-Santos G, Marques TA, Björklund M, Santos-Reis M (2017) Mediterranean mesocarnivores in spatially structured managed landscapes: community organisation in time and space. Agric Ecosyst Environ 237:280–289. https://doi.org/10.1016/j.agee.2016.12.037

    Article  Google Scholar 

  • Direcção Geral do Território (DGT) (2010) Carta de Uso e Ocupaçao do Solo de Portugal Continental para 2007 (COS2007 N5) WMS. 87

  • Díaz-Ruiz F, Delibes-Mateos M, García-Moreno JL, López-Martín JM, Ferreira C, Ferreras P (2013) Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula. Mammal Rev 43:59–70. https://doi.org/10.1111/j.1365-2907.2011.00206

    Article  Google Scholar 

  • Dochtermann NA, Jenkins SH (2011) Developing multiple hypotheses in behavioral ecology. Behav Ecol Sociobiol 65:37–45. https://doi.org/10.1007/s00265-010-1039-4

    Article  Google Scholar 

  • Dormann CF, McPherson JM, Araújo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, Kühn I, Ohlemüller R, Peres-Neto PR, Reineking B, Schroder B, Schurr FM, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography (Cop) 30:609–628

    Article  Google Scholar 

  • Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159

    Article  Google Scholar 

  • Everpidou N, de Figueiredo T, Mauro F, Tecim V, Vassilopoulos A (eds) (2010) Natural heritage from east to west. Springer, Berlin

    Google Scholar 

  • Filipe AF, Cowx IG, Collares-Pereira MJ (2002) Spatial modelling of freshwater fish in semi-arid river systems: a tool for conservation. River Res Appl 18:123–136. https://doi.org/10.1002/rra.638

    Article  Google Scholar 

  • Fisher JT, Wilkinson L (2005) The response of mammals to forest fire and timber harvest in the North American boreal forest. Mammal Rev 35:51–81. https://doi.org/10.1111/j.1365-2907.2005.00053

    Article  Google Scholar 

  • Fowler J, Cohen L, Jarvis P (1998) Practical statistics for field biology. John Wiley & Sons, Chichester

    Google Scholar 

  • Gheler-Costa C, Lyra-Jorge MC, Verdade LM (2016) Biodiversity in agricultural landscapes of southeastern Brazil. De Gruyter Open Ltd, Warsaw

    Book  Google Scholar 

  • Gittleman JL (1989) Carnivore behavior, ecology, and evolution. Springer US, New York

    Book  Google Scholar 

  • Gosselink TE, Van Deelen TR, Warner RE, Mankin PC (2007) Survival and cause-specific mortality of red foxes in agricultural and urban areas of Illinois. J Wildl Manage 71:1862–1873

    Article  Google Scholar 

  • Hersteinsson P, Macdonald DW (1992) Interspecific competition and the geographical distribution of red and Arctic foxes Vulpes vulpes and Alopex lagopus. Oikos 64:505–515. https://doi.org/10.2307/3545168

    Article  Google Scholar 

  • Hipólito D, Santos-Reis M, Rosalino LM (2016) European badger (Meles meles) diet in an agroforestry and cattle ranching area of Central-West Portugal. Wildl Biol Pract 12:1–13. https://doi.org/10.2461/wbp.2016.eb.1

    Article  Google Scholar 

  • ICNF, 2017a. Parques Naturais [WWW Document]. URL: http://www.icnf.pt/portal/ap/p-nat. Accessed 31 January 2018

  • ICNF, 2017b. Rede Nacional de Áreas Protegidas [WWW Document]. URL: http://www.icnf.pt/portal/ap. Accessed 31 January 2018

  • Kalle R, Ramesh T, Qureshi Q, Sankar K (2014) Estimating seasonal abundance and habitat use of small carnivores in the Western Ghats using an occupancy approach. J Trop Ecol 30:469–480

    Article  Google Scholar 

  • Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263. https://doi.org/10.1127/0941-2948/2006/0130

    Article  Google Scholar 

  • Lanszki J, Zalewski A, Horvath G (2007) Comparison of red fox Vulpes vulpes and pine marten Martes martes food habits in a deciduous forest in Hungary. Wildl Biol 13:258–271. https://doi.org/10.2981/0909-6396(2007)13[258:CORFVV]2.0.CO;2

    Article  Google Scholar 

  • Lewis JC, Sallee HL, Golightly RT (1993) Introduced red fox in California. California Department of Fish and Game, Nongame Bird and Mammal Section Report 93-10, Sacramento, USA

  • Lucherini M, Lovari S, Crema G (1995) Habitat use and ranging behaviour of the red fox in a Mediterranean rural area: is shelter availability a key factor? J Zool (Lond) 237:577–591. https://doi.org/10.1111/j.1469-7998.1995.tb05016.x

    Article  Google Scholar 

  • Lüdecke D (2019) sjstats: Statistical Functions for Regression Models (Version 0.17.5). https://doi.org/10.5281/zenodo.1284472

  • Mackenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Academic Press, San Diego, CA

    Google Scholar 

  • MacNally RC (1995) Ecological versatility and community ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Manel S, Williams HC, Ormerod SJ (2001) Evaluating presence—absence models in ecology: the need to account for prevalence. J Appl Ecol 38:921–931

    Article  Google Scholar 

  • Martin J, Basille M, Van Moorter B, Kindberg J, Allainé D, Swenson JE (2010) Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos). Can J Zool 88:375–883

    Article  Google Scholar 

  • Matos HM (2012) Marta (Martes martes): Uma trepadora exímia. In: Loureiro F, Pedroso NM, Santos MJ, Rosalino LM (eds) Um olhar sobre os carnívoros portugueses. Carnivora, Lisboa, Portugal, pp 121–129

  • Monterroso P, Brito JC, Ferreras P, Alves PC (2009) Spatial ecology of the European wildcat in a Mediterranean ecosystem: dealing with small radio-tracking datasets in species conservation. J Zool (Lond) 279:27–35

    Article  Google Scholar 

  • Monterroso P, Castro D, Silva TL, Ferreras P, Godinho R, Alves PC (2012) Factors affecting the (in)accuracy of mammalian mesocarnivore scat identification in South-Western Europe. J Zool 289:243–250. https://doi.org/10.1111/jzo.12000

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x

    Article  Google Scholar 

  • Nowark RM (2005) Walker’s carnivores of the world. Johns Hopkins University Press, Baltimore, MD

    Google Scholar 

  • Oliveira Baptista F (2003) Portugal rural: territórios e dinâmicas. Gab Planeam e Política Agro-Alimentar 1–14

  • Palomo LJ, Gisbert J, Blanco JC (2007) Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, Madrid

    Google Scholar 

  • Pandolfi M, Forconi P, Montecchiari L (1997) Spatial behaviour of the red fox (Vulpes vulpes) in a rural area of Central Italy. Ital J Zool 64:351–358. https://doi.org/10.1080/11250009709356222

    Article  Google Scholar 

  • Pereira P, Alves da Silva A, Alves J, Matos M, Fonseca C (2012) Coexistence of carnivores in a heterogeneous landscape: habitat selection and ecological niches. Ecol Res 27:745–753. https://doi.org/10.1007/s11284-012-0949-1

    Article  Google Scholar 

  • Powell RA (2000) Animal home ranges and territories and home range estimators. In: Boitani L, Fuller T (eds) Research techniques in animal ecology: controversies and consequences. Columbia University Press, New York

    Google Scholar 

  • Quantum GIS Development Team (2016) Quantum GIS geographic information system. Open Source Geospatial Foundation Project

  • R Core Team (2017) R: a language and environment for statistical computing. In: R Found. Stat. Comput. https://www.r-project.org. Accessed 1 Jul 2017

  • Recio MR, Arija CM, Cabezas-Díaz S, Virgós E (2015) Changes in Mediterranean mesocarnivore communities along urban and ex-urban gradients. Curr Zool 61:793–801

    Article  Google Scholar 

  • Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Müller M (2011) pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12:77

    Article  Google Scholar 

  • Rosa García R, Fraser MD, Celaya R, Ferreira LMM, García U, Osoro K (2013) Grazing land management and biodiversity in the Atlantic European heathlands: a review. Agrofor Syst 87:19–43. https://doi.org/10.1007/s10457-012-9519-3

    Article  Google Scholar 

  • Ruiz-Olmo J (2012) Conhecendo melhor a ordem dos mamíferos carnívoros. In: Loureiro F, Pedroso NM, Santos MJ, Rosalino LM (eds) Um olhar sobre os carnívoros portugueses. Carnivora, Lisboa, pp 1–17

  • Salas-Eljatib C, Fuentes-Ramirez A, Gregoire TG, Altamirano A, Yaitul V (2018) A study on the effects of unbalanced data when fitting logistic regression models in ecology. Ecol Indic 85:502–508. https://doi.org/10.1016/j.ecolind.2017.10.030

    Article  Google Scholar 

  • Sales-Luís T (2012) Arminho (Mustela erminea): símbolo de reis. In: Loureiro F, Pedroso NM, Santos MJ, Rosalino LM (eds) Um olhar sobre os carnívoros portugueses. Carnivora, Lisboa, pp 55–65

  • Santos MJ (2010) Conservation planning of oak woodlands in Portugal and California: a multidisciplinary approach. University of California Davis, Davis

    Google Scholar 

  • Santos MJ, Santos-Reis M (2010) Stone marten (Martes foina) habitat in a Mediterranean ecosystem: effects of scale, sex, and interspecific interactions. Eur J Wildl Res 56:275–286. https://doi.org/10.1007/s10344-009-0317-9

    Article  Google Scholar 

  • Silva AP, Curviera-Santos G, Kilshaw K, Newman C, Macdonald DW, Simões L, Rosalino LM (2017) Climatic conditions and anthropogenic factors determine site occupancy in a range-edge badger population: implications for conservation under environmental change. Divers Distrib 23:1–13. https://doi.org/10.1111/ddi.12564

    Article  CAS  Google Scholar 

  • Silva AP, Kilshaw K, Johnson PJ, Macdonald DW, Rosalino LM (2013) Wildcat occurrence in Scotland: food really matters. Divers Distrib 19:232–243

    Article  Google Scholar 

  • Sinclair SJ, White MD, Newell GR (2010) How useful are species distribution models for managing biodiversity under future climates? Ecol Soc 15:8

    Article  Google Scholar 

  • Stoate C, Báldi A, Beja P, Boatman ND, Herzon I, van Doorn A, de Snoo GR, Rakosy L, Ramwell C (2009) Ecological impacts of early 21st century agricultural change in Europe—a review. J Environ Manag 91:22–46. https://doi.org/10.1016/j.jenvman.2009.07.005

    Article  CAS  Google Scholar 

  • United Nations Department of Economic and Social Affairs (2014) World urbanization prospects: the 2014 revision, highlights. New York

  • van Erkel AR, Pattynama PMT (1998) Receiver operating characteristic (ROC) analysis: basic principles and applications in radiology. Eur J Radiol 27:88–94

    Article  Google Scholar 

  • Virgós E, Zalewski A, Rosalino LM, Mergey M (2012) Habitat ecology of Martes species in Europe: a review of the evidences. In: Aubry KB, Zielinski WJ, Raphael MG et al (eds) Biology and conservation of martens, sables, and fishers. A new synthesis. Cornell University Press, USA, Ithaca, pp 255–266

    Google Scholar 

  • Zabala J, Zuberogoitia I, Martínez-Climent JA (2009) Testing for niche segregation between two abundant carnivores using presence-only data. Folia Zool 58:385–395

    Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA (2009) Mixed effects models and extensions in ecology with R. Springer-Verlag, New York

    Book  Google Scholar 

Download references

Acknowledgements

We are grateful to all the people and institutions that provided valuable assistance, particularly Instituto da Conservação da Natureza e das Florestas (ICNF).

Funding

Co-author Eduardo Ferreira was supported by a post-doctoral grant from FCT (Program POPHQREN, ref.: SFRH/BPD/72895/2010). We would like to thank the financial support from the University of Aveiro (Department of Biology), to CESAM (UID/AMB/50017), the FCT/MEC through national funds and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luís Miguel Rosalino.

Additional information

Communicated by: Dries Kuijpe

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 36.3 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alexandre, M., Hipólito, D., Ferreira, E. et al. Humans do matter: determinants of red fox (Vulpes vulpes) presence in a western Mediterranean landscape. Mamm Res 65, 203–214 (2020). https://doi.org/10.1007/s13364-019-00449-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-019-00449-y

Keywords

Navigation